Gallistel 1981 - Organization of Action

THE BEHAVIORAL AND BRAIN SCIENCES (1981) 4, 609-650Printed in the United States ot America

Precis of GallistePsThe organization of action:A new synthesis

C. R. GatlistelDepartment of Psychology, University of Pennsylvania, Philadelphia, Pa.19104

Abstract: The book describes three elementary units of action - the reflex, the oscillator, and the servomechanism - and theprinciples by which they are combined to make complex units. The combining of elementary units to make complex units givesbehavior and the neural circuitry underlying behavior a hierarchical structure. Circuits at higher levels govern the operation oflower circuits by selective potentiation and depotentiation: by regulating the potential for operation in lower circuits - raisingthe potential for some and lowering it for others - a higher unit establishes the overall pattern to be exhibited in the combinedoperations of the lower units, while leaving it to the lower units to determine the details of the implementation of this pattern. Atheory of motivation of the kind long championed by ethologists and physiological psychologists grows out of the notion of theselective potentiation and depotentiation of hierarchically structured units of behavior. The question then becomes how thisconception of motivation may be integrated with a conception of a learned representation of the world to yield a theory of howanimals produce novel motivated behavioral sequences based on learned representations. The representation of space, which iscentral to the behavior of organisms at least as lowly as the digger wasp, is a promising domain for the investigation of thisquestion. Another promising area is the representation of skilled movements, such as handwriting. A number of issues incognitive and developmental psychology are illumined by this theory about the organization of action. Among these are thedegrees-of-freedom problem, the role of practice in development and in the learning of skilled action, and the role of mentalrotation of spatial representations.

Keywords: action; hierarchical structure; motivation; motor organization; oscillators; potentiation; reflexes; representations;servomechanisms; units of behavior

In his penetrating history of nineteenth-centuryneuropsychology, Robert M. Young (1970) observesthat "the most fundamental and perplexing problem inpsychology has been, and remains, the lack of anagreed set of units for analysis comparable to theelementary particles in physics and the periodic tableof elements in chemistry" (p. viii). In The organizationof action: A new synthesis I build the argumentaround a description of three distinct kinds of elemen-tary units of behavior - the reflex, the oscillator, andthe servomechanism. My purpose is threefold. I want tointroduce students to these units by reprinting andexplicating classic papers that delineate the propertiesof these units and the principles governing their inter-action. I also want to place the traditional theory ofmotivation held by ethologists and many physiologicalpsychologists (the drive or instinct theory) on a firmfoundation, by showing that it emerges inescapablyfrom a consideration of the principles by whichcomplex behavior is built up from simple pieces ofbehavior. Lastly, I want to begin the process of inte-grating this view with modern work in cognitive anddevelopmental psychology. A concern for discoveringappropriate units of analysis runs through the wholebook.

Metaphysics

I begin the book with a short exposition of the material-ist metaphysics that is implicit in most modern behav-ioral neurobiology. This metaphysical postulate is thatthe central nervous system is the organ of thought andaction, in just the sense in which the heart is the organof circulation. The explanation of the patterns that wesee in animal action, no matter which animal and nomatter how purposive and intelligent the pattern, is tobe sought in the anatomical structure and physiologicalfunctioning of the animal's central nervous system.While most but not all (cf. Eccles 1980) neurobehav-ioral scientists probably subscribe to this view today, itis seldom made explicit, perhaps. because modernphilosophy has not found any very satisfying way toreconcile it with our conception of ourselves as morallyresponsible actors. I make the materialist assumptionexplicit in the hope that the resultant underlying meta-physical tension will add to the interest of the rest ofthe book.

A commitment to a reductionist analysis - an expla-nation of behavior first in terms of anatomy andphysiology and ultimately in terms of physics andchemistry - is latent in a materialist stance. Despite my

e 1981 Cambridge University Press 0 H0-525X/81/040609-42/$04.00/0 609

Gallistel: Organization of action

reductionist commitment, the book contains relativelylittle anatomy and neurophysiology. A reductionistanalysis is premature until the analysis of behavioralphenomena has identified suitable behavioral units anddetermined the principles to which the physiologicalprocesses underlying those units must adhere. Youcould not have a molecular explanation of the phenom-ena of inheritance in the absence of the concept of agene; no Mendel: no Watson and Crick.

The reflex

The second chapter begins with the work of one of thegreatest of behavioral physiologists, Sir Charles Sher-rington. Sherrington studied behavior - reflexive be-havior — with a view to inferring the underlying neuro-physiology; this, according to my definition, is behav-ioral physiology. In the first chapter of The integrativeaction of the nervous system, which is reprinted inedited form, Sherrington (1906, 1947) establishedseveral pivotal conceptions:

He laid down the criteria for recognizing somethingas an elementary unit of behavior. A unit of behavior isa naturally occurring effector action (muscular or glan-dular) for which we can specify or hope to specify theeffectors involved, the pathways by which the action-initiating signals are conducted to the effectors, and thesource of these signals. In short, a unit of behavior hasthree kinds of sub-behavioral constituents - effectors,conductors, and initiators. A unit is elementary if itcannot be analyzed into constituents that are them-selves units of behavior. The tendon jerk reflex is a unitof behavior (though whether it normally functions as areflex still remains to be decided). The initiator constit-uents are the stretch receptors in the intrafusal organsembedded in the muscle; the conductors are the laafferents from the muscle to the spinal cord and thea-motor neurons from the spinal cord back to themuscle; and the effectors are the muscle fibers. Thetendon jerk reflex is an elementary unit of behaviorbecause its constituents are not themselves units ofbehavior. The motor unit - an a-motor neuron and themuscle fibers it innervates - is not a unit of behavior,because this sub-behavioral unit of analysis lacks aninitiator constituent. In mammals at least, a-motorneurons are not under natural circumstances the sourceof the action-initiating signals. Sensory receptors arethe source of action-initiating signals in the reflex, butby themselves they are also not a unit of behavior,because they lack the effector constituent (and oftenany conductor constituent, as well). The coordinatedstepping of the limbs in locomotion is also a unit ofbehavior, but not an elementary unit, because it maybe analyzed into constituents - the stepping of eachleg - that are units of behavior in their own right.

Sherrington made the following inferences: (1) Toaccount for the specificity of the stimuli required toelicit a given reflex, it is necessary to suppose that thereceptors act as filters selectively tuned to certain kindsof stimuli. (2) To account for temporal summation seenin the elicitation of reflexes, it is necessary to supposethat there exist in the reflex arc physiological processeswhose sluggish rise and fall make them capable ofsummating the effects of signals arriving several

seconds apart. (3) To account for the fact that twosignals starting out from different receptors maysummate to produce a signal to the effectors, it isnecessary to suppose that the reflex arc has a regionwhere the effects of signals arriving via differentpathways may be combined. (4) From the fact that asignal originating at one site may cancel the excitatoryeffect of a signal originating at another site, it isnecessary to suppose that the summation of incomingsignals in the CNS (central nervous system) may beeither additive or subtractive. (5) From the fact thattwo inputs, neither of which is alone capable of elicit-ing any effector action, may together elicit a vigorousaction, it is necessary to suppose that these summationprocesses occur beneath a threshold, a signal going tothe effector only when the sum exceeds the threshold.

Sherrington made the further (and then controver-sial) assumption that the recently propounded celltheory applied to the nervous system as -well. Puttingthis assumption together with the above five infer-ences, he arrived at his conception of the synapse - abrilliantly successful example of inference from behav-ior to underlying physiology, which has stood the testof time very well indeed.

Combinatorial principles

Chapter 3 expounds Sherrington's combinatorial prin-ciples. The first of these was the principle of thecommon path. In propounding this principle, Sherring-ton called attention to the fact that higher units in thenervous system act by way of a common pool of lowerunits. At the level of elementary units, this means thatall the reflexes for a given limb make use of the samemotor neurons. But Sherrington pointed out (onanatomical grounds) that the same principle applied athigher levels. Higher levels did not have direct accessto the motor neurons. They achieved their influence oneffector action by way of the control they exerted overintermediate units. These intermediate units were alsocommon paths, because they were controlled bydiverse and competing higher-level signals. I term thisthe lattice hierarchy principle because when thecontrol of lower units by higher units is diagrammed,the diagram looks like a ramshackle lattice (Figure 1).

Sherrington goes on to identify various coordinativephenomena such as induction and irradiation and to

Figure 1. The distinction between a lattice hierarchy (A)and a partition hierarchy (B). The system underlying thegeneration of animal action is a lattice hierarchy.

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explain them in terms of nonlinear summation atsynapses. He points out that the common path (latticehierarchy) principle requires mechanisms for deter-mining which of the many competing higher units hascontrol of a common pool of subordinate units at anymoment. He recognizes two principles mediating thisintralevel competition for control: mutual facilitationbetween agonistic units and reciprocal inhibitionbetween antagonistic units. He recognizes that theseprinciples apply at the motor neuron level (reciprocalinnervation of antagonist muscles) and at higher levels(reciprocal inhibition between competing reflexes).Lastly, Sherrington appeals to the reflex-chaining prin-ciple to explain sustained sequences of functionallycoherent acts. I argue that this last principle, whilecertainly important in some instances, is not the magicwand it has been taken to be. It does not go very fartoward explaining the structure of most complexbehavioral sequences.

Oscillators

Sherrington thought of the coordinative function of thenervous system entirely in terms of the conduction ofsignals from receptors to effectors, with allowancemade for the addition and subtraction of conductedsignals in the CNS. To imagine that the CNS initiatedsignals in the absence of any sensory provocation nodoubt smacked too much of vitalism. Although Sher-rington was a dualist, he thought the soul initiatedneural activity in the brain, not in the spinal cord. Heknew that the rhythmic, patterned contraction of theheart muscle was driven by signals originating withinthe heart, but he did not consider (until much later) thenotion that the other rhythmic effector actions, whosepervasiveness he clearly recognized, could be driven bysignals from rhythmic signal generators (pacemakers)in the CNS. Sherrington's immediate successor in mypantheon of great behavioral physiologists is Erich vonHoist (1939), who did for the oscillator what Sherring-ton did for the reflex. He followed Graham Brown's(1914) lead in recognizing oscillators as a distinct kindof elementary unit. He also discovered the principle bywhich oscillator outputs combine and the principle bywhich oscillators interact. His paper "On the nature oforder in the central nervous system" is reprinted andexplicated in chapter 4. [See Selverston: "Are CentralPattern Generators Understandable?" BBS 3(4) 1980.]

Von Hoist recognized that most rhythmic effectoractions are not driven by rhythmic stimuli. The rhyth-mic waving of the fins in his favorite experimentalpreparation - a fish with a transection just above themedulla - is not driven by any stimulus that is specificto that action; it is spontaneous. The rhythmic signals tothe effectors have their source in populations of pace-maker neurons in the CNS (or possibly in pacemakercircuits). [See Selverston: Are Central Pattern Genera-tors Understandable?" BBS 3(4) 1980.] These neuralmetronomes may put out their neural ticks and tocks inthe absence of any sensory input. An oscillator is anelementary unit of behavior in which a pacemaker isthe source of signals that drive a rhythmic effectoraction.

Von Hoist recognized that both simple (quasi-

sinusoidal) and complex rhythms were common. Heshowed by closely argued experimental observationsthat complex oscillations in fish fins resulted from thesuperimposition of the outputs of two or more simpleoscillators. He went on to show the same phenomena inmammals, including man. Since the principle ofFourier synthesis - superimposing simple oscillations toachieve movements of arbitrary complexity - isunfamiliar to many neurobehavioral scientists, itreceives a detailed explication in the section that intro-duces von Hoist's paper.

Von Hoist observed, however, that not all perturba-tions in the rhythm of a fish fin could be accounted forby superimposition of oscillator outputs; some were theconsequence of an interaction between oscillators. Herealized that this interaction was what kept one oscilla-tor coordinated with another. He studied the interac-tion (which he called the magnet effect) and adducedthe principle of phase-dependent acceleration/deceler-ation. This principle specifies the manner in which anoscillator responds to a timing signal from anotheroscillator (either internal or external). The response tothe timing signal depends on the phase of the receivingoscillator at the moment the signal is received. Duringsome phases, the timing signal accelerates the receivingoscillator; during others it decelerates it. The plot of thereceiving oscillator's acceleration/deceleration as afunction of the phase at which the timing signal arriveshas come to be called the phase-response curve. So faras I know, von Hoist was first to make such plots. Hepointed out that the phase-response characteristics ofan oscillator determine the phase relationship betweensender and receiver.

Von Hoist's inferences, like Sherrington's, have beenamply confirmed by subsequent electrophysiologicalwork. The concept of coupled oscillators - oscillatorsthat maintain a phase relationship by the exchange oftiming signals - is a cornerstone of modern explana-tions of the neurobiological basis for a variety ofcomplex rhythmic behaviors. The realization of howpervasive rhythmic action is in behavior, a point thatSherrington himself stressed, grows every year.

Locomotion and thedegrees-of-freedom problem

Chapter 5 maintains the theme taken up in chapter 4by reprinting and explicating Wilson's (1966) paper oninsect locomotion, which owed much to von Hoist'swork. This gets a little ahead of the argument, becauseit introduces a complex unit of behavior, locomotion,before an account of the third kind of elementary unit,the servomechanism; but the connection between vonHoist's work and Wilson's is so direct that it seemed ashame to let the thread drop.

Wilson's model, which is the direct ancestor of morerecent models (e.g., Pearson 1976), is a coupled-oscilla-tor model. Each of the insect's six legs has its ownoscillator, which drives the stepping of the leg. In theversion of the model that I elaborate, the leg-steppingcommands from the oscillator are modified by twoother elementary units of behavior. One is an inhibi-tory reflex, which prevents the initiation of a leg swingwhen other legs have failed to take up the load. The

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other is a servomechanism, which adjusts the strengthof the signals sent to the muscles of support andpropulsion so as to compensate for variations in theload to be supported and moved. While there is someexperimental justification for positing the existence ofeach of these components, their precise nature is ratherunclear at present. I include them largely for didacticreasons - in order to illustrate the multilayered charac-ter of the hierarchical structure underlying complexunits of behavior: the combination of the oscillator, thetrigger-inhibiting reflex, and the load-compensatingservomechanism forms a complex unit that controls thestepping of a single leg. The combination of six of thesecomplex units, one for each leg, forms a more complex,higher-level unit that generates locomotion in aninsect.

Modern explanations of locomotion bear directly ona central problem in the understanding of action - theextraordinarily diverse ways in which seeminglyunitary acts achieve expression in muscular contrac-tion. A cockroach's walking straight ahead may seem asimple and unitary act, but the close observer ofcockroaches will note that they have a great manydifferent ways of doing it. There are so many differentleg-stepping patterns that it is only a slight exaggera-tion to say that the cockroach never walks in exactlythe same way twice in its life. By "exactly the sameway" I mean an exact duplication of the timing andmagnitude of contraction and relaxation in every oneof the many muscles involved, over several completestepping cycles.

Animals, unlike most machines, do the same thing inmany different ways, each way peculiarly suited to thecircumstances of the moment. This is part of the reasonwe are loath to believe that animals really aremachines. The problem is to account for this circum-stance-adapted diversity of output without positing asmany different neural curcuits as there are outputs tobe explained. This is the degrees-of-freedom problem,or one aspect of it. Another aspect of the problem is toexplain how higher levels may select among anendlessly rich set of possible lower-level outputs with-out getting bogged down in specifying every detail. Athird aspect of the problem, one that has often preoccu-pied philosophers, is the question of why we arejustified in regarding an act like walking as basicallythe same act from one occasion to the next when, uponmore minute observation, there are so many differ-ences from occasion to occasion. Modern models oflocomotion shed light on all these aspects of thedegrees-of-freedom problem.

Wilson points out that four motor constanciesemerge from an analysis of the bewilderingly diverseinsect gaits: (1) If you focus your attention on just thelegs on one side of the body, you find that in all gaitsthere is a wave of forward swings that progresses fromback to front. First the hindleg swings, then the middleleg, then the foreleg. (2) The duration of a swing isalmost constant; only the duration of the support phaseof a step varies. (3) The interval between the swing ofthe hindleg and that of the middle leg is constant, as isthe interval between the swing of the middle leg andthe foreleg. (4) Turning now to the phase relationbetween legs, one finds a final constancy: legs on

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Figure 2. Black bars indicate the sequence of leg swings onthe left (Li - left front, L2, L3) and right (R,, R2, R3) sides inslow-moving and scurrying insect gaits. Both gaits conform tofour motor constancies: (1) the sequence of leg swings on agiven side progresses from back to front (arrow a); (2) theduration of a leg swing is fixed (interval b)\ (3) the lagsbetween hind- and middle-leg swings and between middle-and front-leg swings are fixed (interval c); (4) opposing legsswing 180° out of phase (the ratio d/e - 1/2). The specifica-tion of the period from one swing of a leg to the next (intervale) exhausts the degrees of freedom in the parameterization ofthese gaits, given the constraints imposed by the four constan-cies. All other differences follow from this specification. Thestepping frequency is 1/e (after Wilson 1966).

opposite sides of the same body segment always step inalternation - that is, 180° out of phase.

These four constancies leave only one degree offreedom - the stepping frequency, which is the recip-rocal of the period from one swing of a leg to the nextswing of the same leg (see Figure 2). Wilson shows thatall the different basic gaits are the consequence ofdifferent values for this one variable.

Modern models of insect locomotion translate eachof the constancies into a structural feature of themodel. The swing signal initiated by the pacemaker isassumed to have a fixed duration, hence the constancyof the swing interval. The pacemaker for the hindleg isassumed to send a timing signal to the pacemaker forthe middle leg in such a way that the middle legpacemaker lags behind the hindleg pacemaker by afixed interval. Likewise for the foreleg pacemaker; it ismade to lag behind the middle leg pacemaker by afixed interval. The fixed-lag coupling between eachoscillator and the ipsilateral oscillator to the rear of itexplains both the back-to-front wave of swings and thefixed interswing intervals within the wave. Lastly, thepacemakers on opposite sides of the same bodysegment are assumed to be coupled 180° out of phase.

The higher levels of the insect nervous system canspecify any gait that circumstances require by meansof a single command signal, a signal that sets thestepping frequency of all the oscillators to about thesame value. This signal raises or lowers the weights onthe metronomes, so to speak, thereby causing them tocycle slowly or rapidly. All the differences that may benoted among the basic gaits are a consequence ofchanging this one parameter in the locomotorymachinery. This is why the small brain of an insectdoes not get bogged down in instructing the lowerlevels on how to go about walking at the rate it wants.



This is also why we are justified in regarding the manydifferent gaits as diverse manifestations of a singleunderlying system.

Finally, the trigger-inhibiting reflex and the load-compensating servomechanism act to adapt the basicgaits to the vicissitudes of walking, the slips and trips,the up-walls and down-walls. That is why the diversityof stepping patterns takes on the character of intelli-gence - the adaptation to momentary circumstances soas to preserve overall function. The best-known exam-ple of this adaptation is the insect's adaptation toamputation of its middle legs. The cockroach normallyruns with a tripodal gait (bottom of Figure 2), in whichthe hind and front legs on one side are swung simulta-neously. When its middle legs are amputated, render-ing this pattern of hind and foreleg activation inadvis-able, the roach switches immediately to a gait in whichthe hind and front legs on a side no longer swingsimultaneously, the so-called diagonal gate of a tetra-pod. This is wired-in intelligence, not learning.

Servomechanisms

Chapter 6 returns to the elementary units of behaviorto describe a third kind, the servomechanism. Aservomechanism, like a reflex, has sensory receptors asat least one source of action-initiating signals. What setsa servomechanism apart from a reflex is the fundamen-tal role of negative feedback in the functioning of theservomechanism. The test of whether a unit is aservomechanism is to disrupt whatever feedback theremay be and see if this disruption alters the operation ofthe unit.

The characteristics of the neural circuitry underly-ing a servomechanism are comprehensible only if onebears in mind the role of the negative feedback fromoutput to input. The clearest illustration of the differ-ence between reflex and servomechanistic neuralcircuitry comes from work that I became aware of toolate to put in the book. Baarsma & Collewijn (1974)subjected both the vestibulo-ocular reflex and the opto-kinetic reaction to analysis by linear systems methods.The vestibulo-ocular reflex is a counter-rotation of theeyes in response to a rotation of the head sensed byreceptors in the semicircular canals. It functions tostabilize the retinal image during head rotations. Thereis no feedback from output to input, because eyerotation has no effect on the semicircular canals. Theoptokinetic reaction is a rotation of the eyes in thedirection of image slippage. It is initiated by circuits inthe retina sensitive to the slippage of the visual image.It, too, functions to stabilize the retinal image duringhead rotation. It, however, is a servomechanism. Therotation of the eyes in the direction of image slippagereduces the slippage that is the stimulus for the rota-tion. This negative feedback through the environmentfrom the unit's output to its input is essential to thenormal operation of the unit.

Baarsma and Collewijn, working with the rabbit,measured the gain in both the vestibulo-ocular circuitand the optokinetic circuit; that is, they measured theangular velocity of the eye rotation elicited by a givenangular velocity of either head rotation or image slip-page. In order to compare directly the characteristics

of the neural circuits per se, it was necessary to preventthe negative feedback from eye rotation to imageslippage, which is a normal part of the servocircuit'saction. This they did by fixing one eye, which looked ata rotating drum, while leaving the other unfixed butcovered, so that it was free to move, but saw nothing.This arrangement, where one eye sees while the othereye moves, forces the neural circuitry underlying theoptokinetic reaction to function as a reflex, with nonegative feedback from its output to its input.

Baarsma and Collewijn found that the gain of thevestibulo-ocular reflex circuit was about .8, whereas thegain of the optokinetic servocircuit was 20-100.Because the output of the servocircuit normallyreduces the stimulus for its own action, it is essentialthat a little stimulus cause a lot of action. This is what again of 20-100 means. When the servocircuit isallowed to function under the negative feedback condi-tions for which it was designed, the high gain in thereceptor-to-effector path makes the unit's normal oper-ating characteristic similar to the operating characteris-tic of the reflex. Both units reduce image slippage by afactor of between 5 and 10. Baarsma and Collewijn alsofound lower acceleration in the servocircuit than in thereflex circuit. Sluggish acceleration (poor high-frequency response) is necessary to preserve theservomechanism's stability - that is, to prevent its goinginto nonfunctional oscillations in response to suddenmovements of the visual image. In short, neuralcircuitry subserving servomechanisms can be expectedto have characteristics that distinguish it from circuitrysubserving reflexes, which is why these should berecognized as distinct kinds of units of behavior.

The taxic orienting behaviors in lower organismswere among the first servomechanisms studied bybehavioral physiologists. One of the pleasures of writ-ing my book was translating for chapter 6 a paper byFraenkel (1927). He shows that the coastal snail isnormally both negatively phototaxic (orients awayfrom light) and negatively geotaxic (orients away fromthe pull of gravity). When the snail crawls on a verticalsurface illuminated from one side, the outputs of theseorienting servomechanisms combine additively, so thatthe snail's trail is the vector sum of a sideways-oriented(negatively phototaxic) crawl and a vertically oriented(negatively geotaxic) crawl.

When the snail is both upside-down and underwater,something fascinating happens. The snail is no longernegatively phototaxic; it is positively phototaxic.Perhaps the most elegant demonstration of both thereversal of the sign of the phototaxis and the vectorsummation of geotaxic and phototaxic orientationscomes from placing the snail on the inside bottom of asubmerged glass cylinder illuminated obliquely (Fig-ure 3). The snail crawls away from the light on anoblique angle to the cylinder's axis. As it mounts theside of the cylinder, the obliquity increases because thegeotaxic orientation gets stronger. As the snail passesthe point halfway up the side of the cylinder, itbecomes upside-down, and the sign of the phototaxisreverses, so that it now crawls along the inside top ofthe cylinder back toward the light.

Fraenkel argues that the snail's taxic orienting mech-anisms go a long way toward explaining how it gets

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obliquelyincident light

Figure 3. Bohn's (1905) experiment demonstrating thevector summation of phototaxic and geotaxic orientations andthe reversal of the sign of the phototaxic orientation when thesnail is upside-down (and underwater).

from the sea floor to where it is usually found - increvasses on coastal cliffs, a few meters above high tide.The reversal of the sign of the phototaxis moves thesnail out along the ceiling of the underwater crevassesin the cliff. Since the reversal occurs only when thesnail is both upside-down and underwater, the snail'sprogression comes to an end in the dark inner recess ofthe first crevasse it comes to above the reach of the sea.

The reversal of the snail's phototaxis is the first ofmany examples of the principle of selective potentia-tion and depotentiation in the organization of behavior.The snail has neural circuitry for both positive andnegative phototaxic orienting, but only one of thesetwo opposing circuits is allowed to be active at any onetime. When the snail is upright, the negatively photo-taxic circuit has the potential to be active. Whether it isin fact active depends on whether there is a lightgradient. When, however, the snail is upside-down andunderwater, the negative phototaxis is depotentiatedwhile the positive phototaxis is potentiated. By control-ling the potential for activation in these orientingcircuits, the higher levels of the nervous system forge afunctionally cohesive sequence of orientations.

Reafference and efference copy

When an animal acts it generates sensory inputs thatare a consequence of its own action. These are termedreafferences, to distinguish them from exafferences,which are sensory inputs that come from events in theoutside world. These reafferences may activate a unitof behavior whose action interferes with the action ofthe original unit. When a fly turns, for example, itnecessarily causes the visual pattern to slip across itsfaceted eye. This should activate the fly's optokineticreaction, producing a turn that counteracts the originalturn. Why does the fly's optokinetic reaction not ineffect paralyze the fly by constantly opposing turnsinitiated by other units?

Von Hoist & Mittelstaedt (1950), whose well-knownpaper "The reafference principle" is reprinted in chap-ter 7, show that interference from the optokinetic unitcan be prevented by cancelling the reafferent input tothat unit with a copy of the efferent (outgoing signal)that initiates a turn. Because the reafference is aconsequence of the fly's own action, it may bepredicted by the signal that commands the turn. Thestrength and sign (left-right) of the signal thatcommands a turn predict the strength and sign of the

signal that the turn will generate in the optical circuitsthat respond to image motion. A left-turn commandwill lead to a visual motion signal of opposite signbecause a left turn causes the visual pattern to sliptoward the fly's right. Therefore, adding a suitablyscaled copy of the left-turn command to the afferentsignal coming into the optokinetic circuit will cancelout the reafferent component of that input, leavingonly the component that reflects movements of theworld rather than movements of the fly.

Von Hoist and Mittelstaedt go on to explore otherkinds of interactions between efferent and reafferentsignals, greatly expanding our sense of the role thatservomechanistic units play in behavior. In the laterparts of the paper, they focus on the perceptual conse-quences of the interplay between reafference andefference copies. The best-known demonstrations thatthe principle of cancellation by efference copy is atwork in the human nervous system come from cases inwhich the response of the eye muscles to efferentsignals is impaired by disease or drugs (e.g., curare). Insuch cases, the motion produced by the efference is lessthan it should be, hence also the reafference from themotion. When the efference copy is added to theweaker-than-usual reafferent, it overmatches it.Instead of cancelling out the reafferent, the efferencecopy inserts a signal of opposite sign into the sensoryperceptual pathway. Hence, when individuals with aperipheral debilitation of the oculomotor apparatuscommand their eyes to look to the right, they perceivethe world as jumping to the right. The efference copyhas generated a perceptual effect all by itself, a percep-tion for which there is no sensory source.

Efference copies are low-level, neurophysiologicallyexplicable instances of expectations. They are centrallygenerated signals that anticipate forthcoming sensorysignals. They are, of course, unconscious expectations.But when these unconscious expectations are violated,the difference between expectation and outcome showsup in conscious experience. Von Hoist and Mittelstaedtgive several other examples of this same phenomenon.[See also Gyr et al.: "Motor-Sensory Feedback andGeometry of Visual Space" BBS 2(1) 1979.]

Hierarchical structure

Chapters 2-7 consider different kinds of elementaryunits of behavior, the principles by which their outputsare combined, and the principles by which the unitsinteract. Chapter 8 turns to a consideration of thehierarchical structure of the system. It reprints anedited version of a lengthy paper by Paul Weiss (1941)on the development of coordinated action in salaman-ders. Much of the developmental part has been editedout, because I wanted to emphasize what Weiss had tosay about coordination itself. He stresses the hierarchi-cal organization of the mechanisms of coordination,distinguishing six levels of coordination up to the levelof simple acts: Level 1 is the motor unit - that is, theindividual motor neuron and the muscle fibers it inner-vates. As already pointed out, this is a sub-behavioralunit of action. Level 2 is the coordination of the motorunits that comprise a muscle. The size principle (Stein1974), which asserts that smaller motor neurons


commanding weaker contractile effects are alwaysrecruited first, is an example of a principle of coordina-tion at this level. This is still a sub-behavioral level ofanalysis. Level 3 is the level of muscle groups - forexample, the antagonistic muscles on either side of ahinge joint. Elementary units of behavior commandmuscle groups, so this is the first behavioral level ofanalysis. Level 4 is the level of the organ. The combina-tion of an oscillator, a trigger-inhibiting reflex, and aload-compensating servomechanism, which togethercontrol the stepping of a single leg, is an example of acomplex unit of behavior at this level. Level 5 is thelevel of the organ system. The unit that coordinates thestepping of all six legs in order to produce forwardlocomotion is an example of a unit at this level. Level 6is the level of the organism as a whole. The units thatproduce oriented progressions, in which an orientingunit operates together with a locomotory unit, areexamples of units at this level.

Weiss's sixth level, the level of simple acts of thewhole organism, may, for convenience at least, beregarded as the level at which the study of sensorimo-tor coordination leaves off and the study of motivatedbehavior begins. Motivated behavior is behavior inwhich many different acts are deployed in such a wayas to achieve a goal or function that no one act achievesby itself. Oriented progressions are salient among theacts that are deployed in the appetitive phase ofmotivated behavior. Other acts - for example, theingestion and rejection acts so carefully analyzed byGrill and Norgren (1978) in the rat - come into playduring the consummatory phase.

The centerpiece of Weiss s paper, for my purposes, ishis compelling demonstration that locomotory systemsat Level 5 of the hierarchy really are treated as units byhigher levels of the salamander's nervous system. Weissinterchanged the forelimbs in larval salamanders, sothat the animals' forelimbs were oriented backwards.These surgically translocated forelimbs were reinner-vated, with the motor neurons appropriate to each kindof muscle finding their way to that muscle in the newbackward-pointing limb. The result was that thepattern of motor neuron signals that would ordinarilystep the forelimbs so as to propel the salamanderforward caused, in the turned-around limbs, a patternthat was unaltered so far as the limbs themselves wereconcerned, but propelled the salamander backward,not forward.

The normal salamander can walk both forward andbackward. For these altered salamanders to do thesame, they would have to instruct their hindlimbs towalk forward while instructing their forelimbs to walkbackward, and vice versa. This they could not do, andnever learned to do. The forelimbs and hindlimbs ofWeiss's salamanders always worked at cross purposes.This is the most compelling demonstration I know ofthe unitary character of higher-level organization inthe motor system. The salamander has a unit thatgenerates forward locomotion; it also has a unit thatgenerates backward locomotion. Each of these unitsgenerates a great diversity of stepping patterns. Thesalamander may call one, or it may call the other, but itcannot call half of one and half of the other. Thediversity in its stepping patterns is delimited by the


unitary hierarchical structure of the systems thatgenerate the patterns.

Weiss makes a severe indictment of most modernwork on learning. Given that one is dealing with ahierarchically structured system for generating behav-ior, one of the most basic questions one can ask aboutthe phenomena of plasticity is, at what level of thehierarchy does the alteration in structure occur? Untilthis question is answered, there is no hope of predictingthe range of behavioral alterations consequent uponthe learned alteration in structure. Wickens (1938,1939), in his studies of response generalization in condi-tioned finger-withdrawal experiments, raised this ques-tion and demonstrated its pertinence. But the questionhas in general been left unanswered - indeed, unad-dressed.

Manifestations of hierarchical structure

Chapter 9 surveys diverse material in order to show,first, the many ways in which the hierarchical structureof the system that generates action becomes manifest inbehavioral experiments, and second, the many cases inwhich one may see the principle of selective potentia-tion and depotentiation at work.

Transaction studies. On anatomical, phylogenetic, andontogenetic (embryological) grounds, it is possible todistinguish five major divisions of the vertebratecentral nervous system - the spinal cord, the hindbrain,the midbrain, the diencephalon, and the forebrain.Transection experiments study the behavioral capaci-ties of animals whose nervous system has been cut at ornear one of the boundaries between major divisions.These experiments reveal a rough correspondencebetween levels of organization in behavior and themajor divisions of the CNS. In the spinal animal, unitsup to Weiss's Level 4 are intact. Fragments of Level 5units are seen, but few units at this level are intact. Inthe hindbrain animal, many Level 5 units are intact ornearly so, but one does not see acts of the wholeorganism. In the midbrain animal, Level 6 units areintact. The animal walks, climbs, grooms, ingests, andso on. But one does not see motivated behavior. Theacts are not deployed in such a way as to serve theanimal's fundamental requirements - the preservationof the milieu interne, defense, and reproduction. Inthe animal whose diencephalon and immediately adja-cent tissue have been spared by the transection orablation, one sees motivated behavior. The devastatingloss of the analytic and planning functions in theforebrain makes this motivated behavior veryawkward and frequently poorly oriented, but theanimal does deploy its limited means so as best to serveits nutritive, defensive, and reproductive goals.

Brain stimulation. The lattice hierarchy conception wascentral to some of the most penetrating work ever doneon the behavioral consequences of focal stimulation ofthe brainstem, the work by von Hoist and Ursula vonSt. Paul (1963). They used the lattice hierarchy concep-tion to explain the multiple, seemingly diverse behav-ioral consequences of stimulating one and the samesite, and to explain the fact that the same effects may



be obtained from many different sites. They stress thesupreme importance of a "level-adequate terminolo-gy" - that is, a description of the behavioral effect thataccurately reflects the level of organization at whichthe units activated by the stimulation function. Theypoint out that nothing but confusion and perplexity canresult from lumping together in one functional cate-gory all the sites at which stimulation elicits, for exam-ple, some salient aspect of attack behavior. Some sitesmay function to coordinate that aspect and only thataspect of aggressive or defensive behavior, while othersites may govern a much wider domain, of which thatpiece of behavior is but a component. One must surveythe behavioral effects in a variety of circumstances andknow the animal's patterns of behavior thoroughly ifone is to have any hope of making an adequateassessment of the behavioral function of the tissueexcited by the stimulation. It cannot be said that mostworkers in brain stimulation have taken these stricturesto heart.

Flynn's work (e.g., 1972) on stimulation-elicitedpredation in cats provides superb demonstrations ofselective potentiation in a motivational context.MacDonnell & Flynn (1966) showed that stimulatingthe cats diencephalon unilaterally at sites that inducedcomplete predatory sequences of acts selectively poten-tiated several reflex components of the consummatoryact on the contralateral side of the cat's face. In effect,the side of the cat contralateral to the site of dience-phalic stimulation reacted to prey stimuli in a preda-tory fashion while the ipsilateral side reacted as itwould in a cat not bent on capturing prey. This resultargues strongly, I think, that diencephalic neural tissueachieves its motivating function by way of the selectivepotentiation of acts that subserve a common goal.Beagley & Holley (1977) have extended this finding toa learned act. They showed contralateral potentiationof a learned food-seeking response to a discriminativecue in the rat.

The behavior of hybrids. Dilger's (1962) studies on nestbuilding in hybrid lovebirds show the importance ofinherited units of behavior in determining the outcomeof learning experiments. He interbred two species ofnest-building lovebirds, one of which carries materialto the nest by tucking it in its feathers, the othercarrying it in its bill. The hybrid offspring muchpreferred the feather-tucking approach, even though itnever worked for them (since they did not execute themaneuver well and the material always fell out enroute to the nest).

Operant conditioning. Skinnerians have discovered thatthe inherited organization of behavior really doesmatter in operant conditioning. The Brelands (1961)were among the first to emphasize that operant behav-ior was synthesized from the preexisting species-specific units of behavior that tend to occur in connec-tion with a given kind of reinforcer. When these unitsare not suited to the result the trainer wants to achieve,it is hard going, as Hineline and Rachlin (1969) foundwhen they tried to condition a pigeon to peck a key toescape footshock. Not surprisingly, the birds tried tosolve the problem with a unit of behavior ordinarilymore suited to the goal of escaping painful stimuli to

the feet - flying. The work of Hearst & Jenkins (1975),Thorpe (1963), and Sevenster (1973) has further em-phasized the role that preexisting higher level units ofresponse organization play in instrumental learning.

Development and recovery. The existence of higher-level control over lower-level units of behavior is docu-mented in Hall, Cramer, & Blass's (1977) studies on thedevelopment of suckling in rat pups, in Twitchell's(1970) studies of the development of grasping inhuman infants, and in Teitelbaum's many studies onthe recovery of behavioral function following damageto the CNS in adults (cf. Teitelbaum 1971).

Motivation

Behaviorists, many neurobiologists, and some physio-logical psychologists mistrust the term "motivation."They seem to feel that when we really understandbehavior we won't need to talk about motivation anymore. I think they could not be more mistaken. Theconcept of motivation will play a central role in anysatisfactory account of behavioral causation. There isno getting around the fact that animals pursuedifferent goals on different occasions and that the goalan animal is pursuing determines how it will react, andeven whether it will react at all, to a given stimulus.The cat in pursuit of prey reacts to a touch on the cheekby a turn toward the touch, and to a touch on the lipsby a snapping open of the jaws. A cat not interested inprey turns away from a touch on the cheek and pursesits lips to a touch on the lips.

The study of motivation is the study of the goalsanimals pursue, the acts they can deploy in pursuit ofthose goals, and the processes that determine whichgoals will be pursued and how the acts will bedeployed. I argue in chapter 10 that the principle ofselective potentiation is central to understanding howmotivating signals, arising in and around the dienceph-alon, impose goal-directedness on the animal's behav-ior. I follow the ethologists (Tinbergen 1951; Lorenz1937) and many physiological psychologists (Lashley1938; Morgan 1943; Stellar 1960) in arguing thatcentral motive states (drives) increase the potential forcertain acts and decrease the potential for others. Theyselectively favor the acts that subserve a commonpurpose. In this way, they establish the generaltendency (the goal) of an animal's behavior, whileleaving it to the activating effects of ambient condi-tions on lower-level units to determine just how thegoal is pursued at any given moment.

The behavior controlled by the higher, motivationallevels of the action hierarchy is flexible, adaptable,purposive, and intelligent precisely because of thehierarchical arrangement. The higher levels lay down aframe or general direction for behavior by selectivelypotentiating coherent sets of behavioral options. Theflexibility of the behavior, its variability from occasionto occasion, and its suitability to momentary and unfor-seeable circumstances reflect the fact that what higherlevels establish are options, not requirements. Thehigher levels do not directly command muscles. Theydo not determine which muscles shall contract andwhen. They determine the set of general patterns of



integrated sequences of simple acts that may beobserved when a particular motivational state is inforce. The imposition of a general plan by means ofselective potentiation gives behavior its purposive qual-ity, its long-term functional coherence. Each lowerlevel in the hierarchy specifies more narrowly which ofthe many variations, subvariations, and sub-subvaria-tions of the general plan will actually appear at aparticular moment. Lower levels fill in or determinedetails within the general pattern.

Since the stimuli and conditions that give rise to aparticular drive are a familiar province of physiolog-ical psychology, I devote little space to this topic. I notethat the kinds of processes that determine the waxingand waning of drive signals are analogous to the kindsof processes that give elementary units of behaviortheir distinctive characters. A drive may be elicited bya stimulus; it may have an endogenous oscillatorycomponent; and, of course, the homeostatic drives havemuch to do with negative feedback regulation. Also, asLorenz (1950) has emphasized, the potential for acti-vating some acts may grow simply as a function of theinterval since the act was last performed, quite inde-pendent of all other considerations, to the point wherethe act may occur in a behavioral vacuum - a situationin which there is no stimulus for the act and in which itserves no goal.

The oligarchical problem. Most propounders of thethesis that the system generating behavior has a hierar-chical structure have tried to specify units that consti-tute an oligarchy at the top - the major drives or majorinstincts (cf. Tinbergen 1951). These lists have provedan embarrassment. Many of the acts seen in seminatu-ral conditions do not subserve any major drive (cf.Kavanau 1969; Leyhausen 1965); the conditions oftheir occurrence make such an assumption gratuitous.Also, as Lorenz (1950) first argued, the superordinate-subordinate relationship between units is frequentlyreversible. Rats deprived of water will run in order togain access to water; but rats deprived of running willdrink in order to gain access to a running wheel(Premack 1962). One must recognize that at motiva-tional levels of function in higher vertebrates the hier-archy is labile. Which units subserve which is context-dependent. There is no oligarchy. There is a heterar-chy.

Knowledge and action

What Young (1970) terms the sensorimotor approachto neuropsychology tries to solve the problem of therole of knowledge in the control of action by assumingthat knowledge is an acquired alteration in sensorimo-tor connections. I argue in chapter 11 that this ap-proach has been a failure. Knowledge often enters intothe control of action in such a way as to producebehavior that the animal has never produced beforeand will never produce again. The female digger wasp,after digging an egg-laying burrow, gains knowledgeof its location relative to surrounding landmarks duringa survey flight that she makes before departing on herhunting expeditions. This knowledge enables her tofind her way back to the burrow from an arbitrary

location, even one she is carried to inside a closed box(Thorpe 1950). To speak of her homing behavior as ahabit or as an alteration in her response probabilities isa wave of the hand, because she orients correctly fromrelease sites where she has never been. There iscompelling evidence that she orients by reference tolandmarks, not by reference to any stimulus beaconemanating from the burrow. The conclusion is inescap-able that she has made a representation of thesurrounding territory, a representation that she can useto orient toward the burrow from an arbitrarily chosenpoint within that territory. This conclusion poses twochallenging questions: (1) How shall we describe herrepresentation? (2) What is the process by which thisrepresentation enters into the control of her actions?[See also Griffin: "Prospects for a Cognitive Ethology"BBS 1(4) 1978.]

To illustrate one approach to these questions, Ireview Deutsch's (1960) theory of map-referencednavigation in animals. Deutsch's theory of the repre-sentation assumes only two primitives - points (repre-sentations of distinctive landmarks) and connectionsbetween points (representations, roughly speaking, ofthe order in which the distinctive landmarks areencountered). Formally speaking, Deutsch assumes anetwork or graph-theoretic representation. Deutschassumes that motivational signals enter the network viathe representations of a goal object and propagatedecrementally to all other points via the connectionsbetween points. The decremental propagation of thesignal outwards from the goal point establishes a moti-vational gradient on the representation. At any oneplace in the territory, the animal will perceive only asubset of the points represented on its map. The moti-vational gradient establishes a rank ordering of thesepoints on the basis of their motivational salience. Thatpoint whose representation on the map has the fewestconnections separating it from the goal has the highestmotivational salience. The animal orients toward thepoint of greatest salience and locomotes. This bringsstill more salient points into view. In this way theanimal progresses to the goal.

The above model is likely to make many behavioralneurobiologists squirm. It sounds so nonphysiological,so mentalistic. I review it because, for one thing,Deutsch (1960) actually built a working model. I do notknow of any such attempt by theorists working in thesensorimotor tradition, and I believe that any suchattempt would reveal the bankruptcy of theirapproach. It may also help to remember that theconcept of the gene - self-replicating particle for theconveyance of structure-specifying information fromone generation to the next - did not sound verychemical during the first half of this century.

In any event, I argue in chapter 12 that Deutsch'smodel is probably inadequate, because animals' spatialrepresentations are probably richer than he assumed.Deutsch's model assumes point-to-point navigation.The evidence for dead-reckoning navigation (cf.Carr & Watson 1908; Maier 1929; O'Keefe & Nadel1978; Olton & Samuelson 1976; Tinkelpaugh 1932)implies a representation with a richer set of primitives,the primitives of Euclidean geometry. In dead-reckon-ing navigation, the animal does not perceive the point



to which it is oriented; the orientation and the distanceto be covered are derived from knowledge of therelation between the unperceived point toward whichthe course is set and other perceived points that do notlie on the course. The ability to derive the angle anddistance of the required course would seem to require arepresentation that preserves angle, distance, collinear-ity, parallelism, and the other fundamental propertiesof Euclidean geometry. [See also Olton et al.: "Hippo-campus, Space and Memory" BBS 2(3) 1979; and BBSmultiple book review of O'Keefe & Nadel: "TheHippocampus as a Cognitive Map" BBS 2(4) 1979.]

The theory of action in cognitive psychology

Motor schema. Theorists outside the sensorimotortradition have repeatedly suggested that learned move-ments, such as those made in writing, must be repre-sented by "schemas," "movement formulae," and thelike. This is another one of those cognitive notions thatfill neurobiologists with unease. It seems so vague, andhopelessly remote from neurobiological embodiment.One of the things I try to do in chapter 12 is to give anexplicit statement of what the neural embodiment of amovement schema could look like.

A schema is an abstract representation of the form ofa movement. It is posited to explain the fact that one'shandwriting looks the same whether one writes at adesk or on a blackboard. Since the muscles used and thebiomechanics are radically different in these two writ-ing situations, the form of the movements made inwriting must be specified independently of the motor-neuron signals required to realize the movements.What one wants is a neurobiologically plausible way ofspecifying the trajectory of a movement without speci-fying patterns of motor-neuron activation. Yet theremust be some • way of deriving patterns of motor-neuron activation from this specification of trajectory.

Oscillators are a demonstrated reality in the nervoussystem, as is the principle of superimposing oscillatoroutputs. The Fourier theorem assures us that anytrajectory may be represented as the superposition of -the concurrent execution of - a suitably chosen set ofoscillations. Anyone who has seen a chart of Lissajousfigures will realize that limited modulations of theamplitudes, periods, and frequencies of two concurrentorthogonal oscillations can give rise to an astonishingvariety of trajectories. These considerations make itattractive to assume that oscillations are the primitivesin action schemata - the alphabet in which everyschema is written. Thus, the schema for writing theletter "e" would consist of the specification of therequired modulations in the periods, phases, andamplitudes of two orthogonal oscillations.

At the time I made this extremely speculativesuggestion I was unaware of the recently publishedwork by Hollerbach (1981). I did not know how simpleand elegant an oscillatory theory of handwriting couldbe. Nor did I know that recordings of movements madeduring handwriting and the nature of the distortions inrapid writing make such a theory empirically plausible.On the basis of Hollerbach's work, I am prepared totake the oscillator model of schemata more seriously.

My original purpose was only to show that neurobiolog-ically plausible conceptions of schemata could be imag-ined.

The general outlines of the process for translatingoscillatory letter schemata into movements are fairlyclear. The point on the body that is to execute thetrajectory must be set into at least two concurrentorthogonal oscillatory motions and a left-right linearmotion. All the different letters are generated bymodulating the period, phase, and amplitude of thetwo oscillatory motions. A difficulty that must be dealtwith, however, is the nonlinear biomechanics of thelimbs, to which Bernstein (1967) has called attention. Itwould seem that the translation process must involve alevel that introduces offsetting nonlinearities in themotor-neuron signals (cf. Pew 1974). This may bethought of as tuning the system (Turvey 1977). Theneed to discover appropriate tunings may shed somelight on the role of practice in the acquisition of motorskill.

Euclidean maps and the brain. Humans using an exter-nal map (e.g., a road map) to navigate find it helpful torotate the map until it and the world represented by ithave the same alignment with respect to the naviga-tor's body. When one is driving from San Francisco toLos Angeles, the map is held so that Los Angeles is outtoward the windshield; on the way back, the map isrotated 180°, putting San Francisco toward thewindshield. This quirk highlights the fact that map-referenced navigation requires the interrelation ofthree systems of coordinates - the world system, themap system, and the body system. I speculate thatrecent studies by Cooper & Shepard (1979) andPinker & Kosslyn (1978) on the human capacity torotate mental images of spatial configurations areexamining a phylogenetically ancient process by whichanimals' maps are rotated into alignment with theenvironments they represent in order to make naviga-tional computations simpler.

The fascinating thing about the mental rotationsexamined in these experiments is that they are alwaysand seemingly inescapably continuous. If the brainwishes to rotate the representation 180°, it seems tohave no choice but to do so by passing it through all theintervening angles. This suggests that the physicalembodiment of spatial representations in the brainmust be such that the only natural way to perform therotation operation is continuously. The map that isembodied by a drawing on paper has this property.You cannot rotate it to a new orientation withoutpassing it through the intermediate orientations. Thematrix representations of spatial configuration in acomputer memory, as simulated by Kosslyn, Pinker,Smith, & Schwartz (1979), do not have this property. Inthe matrix embodiment of a spatial representation, therotation operation is carried out by computing a newlocation for the contents of each cell. There is nonatural, unavoidable reason for computing interme-diate locations. Indeed, such computations would seemcounterfunctional in that they ought to increase theerror in the final relocation. [See also Pylyshyn: "Com-putation and Cognition" BBS 3(1) 1980.]

How then could representations of spatial configura-


Commen<ari//Gallistel: Organization of action

tion be embodied in the brain in such a way that thecontinuity of the rotation operation becomes inescapa-ble? One way would be for the perceptual system todecompose the to-be-represented configuration into itsthree-dimensional Fourier components (in effect, torepresent the environment in terms of macroscopicmatter waves, analogous to sound waves). The braincould then store the information about spatial configu-ration in the form of a set of five-dimensional signalvectors. One signal in each vector would specify theperiod of a Fourier component, another its amplitude,and the remaining three its phase and orientation. Ifinformation about spatial configuration were stored inthis fashion, then the rotation operation would have theunavoidable continuity revealed by the mental-imageexperiments. The only natural way to rotate a spatialconfiguration represented in this way is to change thevalues of the signals within each vector that specify thephase and orientation of the component. Changes inthe value of any brain signal are almost certainlycontinuous. The intermediate values that the phase andorientation signals would have to pass through en routeto their new values would specify intermediate orienta-tions.

The exceedingly speculative character of thisconcluding suggestion hardly needs emphasizing. Thesuggestion is put forward only to illustrate a deeplyheld belief: behavioral studies, even studies of mentalimagery, are an indispensable source of clues as to theprimitives in terms of which the brain represents andacts upon the world. If we are to have neurobiologicalexplanations of behavior, we must discover those prim-itives.

ACKNOWLEDGMENTSI dedicate this precis to Donald Kennedy on the occasion ofthe celebration of his fiftieth birthday. He first stimulated myinterest in the neural circuits subserving units of behavior ininvertebrates and has greatly shaped my views. Also to TonyDeutsch, who first drew my interest to the nature of spatialrepresentations and how they control action, and who set thecourse of my research in electrical self-stimulation of thebrain. The expenses of preparing the precis were defrayed byNIH Grant NS 14935.

Stelmach & Requin, 1980 for "the state of the art.") Particu-larly welcome are the reprints of papers by Sherrington(1906), van Hoist (1937), Wilson (1966), Fraenkel (1927), vonHoist & Mittelstaedt (1950), and Weiss (1941). The author'scommentary will help the student better appreciate theseclassic contributions. If Gallistel had chosen the subtitle Clas-sic perspectives I would rest content; but when a book tells melittle that I did not know fifteen years ago, I find the claim ofhis subtitle, A new synthesis, somewhat suspect.

Many ideas concerning "the organization of action" wereintroduced to the Western literature by Peter Greene in thesixties (e.g., 1964, 1967). Yet Green's ideas, far from beingdeveloped systematically by Gallistel, are dismissed in onesentence in a section entitled "The Turvey theory." Turvey issaid to have been influenced by Bernstein and Easton, but (asI am sure Turvey would agree) Turvey s primary influencewas Greene. Greene was one of the first American workers tostress the centrality of the work done by the Russian schoolinitiated by Bernstein, and Easton was Greene's Ph.D.student. I was also disappointed that the work of Bernsteinhimself, and the neurophysiological and robot locomotionstudies of this "descendants" in Moscow, are only mentionedin passing.

Another incredible omission in Gallistel's "new synthesis" isall mention of artificial intelligence, save for the erroneousascription, on page 365, of the notion of heterarchy toMinsky & Papert (1972) rather than to McCulloch (1945).Rather than review this literature, let me simply cite twopapers. Sacerdoti (1974) builds on a number of classic studiesin robotics to study hierarchical planning. This work isapprovingly cited by Shaffer (1980) in his study of the timingand sequencing of action. Again, Kuipers (1978) offers an Alapproach to cognitive maps, while Arbib & Lieblich (1977)counter Gallistel's claim (p. 381) that "Deutsch's (I960)model for the control of action by a cognitive map . . . is . . .the only model that explicitly specifies a physically realizableprocess by which a motivational signal may organize the useof a map." Talking of cognitive maps: I would like to haveseen a thoughtful discussion of the light an action-orientedapproach sheds on the analysis of perception. True, much of aparagraph is devoted to the 1963 work of Held & Hein on therole of activity-induced sensory feedback in behavioral devel-opment, but this is too little too late (p. 378 of 394 pages oftext). [See also Gyr et al.: "Motor-Sensory Feedback andGeometry of Visual Space" BBS 2(1) 1979.]

One final nomination for my (distressingly incomplete) listof ingredients in a genuinely new synthesis: Piaget-inspiredstudies of the role of action in the cognitive development ofthe child. For an excellent review of this approach, seeForman (1981).

Open Peer Commentary

Commentaries submitted by the qualified professional readershipof this journal will be considered for publication in a later issue asContinuing Commentary on this article.

A new synthesis?

Michael A. ArbibComputer and Information Science Department, University of Massachu-setts, Amherst. Mass. 01003

Gallistel's The organization of action is a welcome book, andshould accelerate the growing integration of the study ofmotor behavior into cognitive science and neuroscience. (See

On a clear day you can see behavior

Robert C. BollesDepartment of Psychology, University of Washington, Seattle, Wash.98195

By and large, psychologists have remained totally oblivious tothe good work that has been done by other scientists on theorganization of action. One reason for this curious neglect hasbeen noted by Gallistel. Up until about a dozen years ago, themajority of psychologists, and surely the great bulk ofpsychologists who were concerned with learning, subscribedto the S-R formula. All responses, learned and unlearnedalike, were controlled directly by their controlling stimuli.When learning occurred, it was the action system itself thatbecame modified. Reinforcement and classical conditioningboth resulted in the formation of S-R associations. Today, ofcourse, hardly anyone subscribes to the S-R formula, because


Commentary/Gallistel: Organization of action

there is a new formula to believe in. Everyone (almost) stillbelieves in associationism, and studies association formation,but the new associations are quite different: they are S-Sconnections. When learning occurs now, it is the perceptualsystem, or the memory system, or something of that sort thatis modified. That is all well and good as far as the study oflearning is concerned, but where does it leave our under-standing of behavior? How do we explain the emergence ofnew behaviors when learning has occurred? For that matter,how are we supposed to explain any kind of behavior? How isthe modern psychologist, caught up in the analysis of memoryand the formation and organization of S-S associations, able tosay anything about what the organism is doing? It wouldalmost appear that when we abandoned the old S-R formula,we also turned away from behavior.

The search for appropriate and realistic explanations ofbehavior has always been a serious business, but with thepresent involvment in S-S mechanisms the problem hasbecome all the more serious. It is now an urgent matter.Gallistel has not only seen the problem and tried to start doingsomething about it: he has started off, I believe, in the rightway. He starts with the outside of behavior, the oscillators, thereflexes, the automatisms, and encourages me to believe thathe will ultimately be able to explain a lot of behavior withthese devices. At least, the details of behavior will beexplained at the level at which the detail is relevant. Why thebehavior is occurring at all, is quite a different matter; that isthe inside of behavior, of which I will speak in a moment. Thekey to this approach, of course, is the idea of hierarchicalorganization. We might also call it the principle of localautonomy. Gallistel illustrates the idea in a variety of ways,but I cannot resist another illustration:

One day the word comes down from upstairs at GeneralMotors, "We have a new goal: 300,000 Pontiacs this year."That is all they have to say, because the people at PontiacDivision know what to do. They get orders out to thefactories, start stockpiling materials, get on the phone toPersonnel to hire new people, contact the crew at the SalesDepartment, send a man over to the bank to get credit ready,and so on. Each of these groups knows how to do what itneeds to do, and each of these groups knows how to commandother people down the line to do what they have to do. Whenit is all over, about 300,000 people will have been involved inmaking and selling about 300,000 Pontiacs. The process issimilar in complexity to an animal walking across the room.And it works. I am inclined to believe that it works for thesame reason - namely, that such a complex operation can onlybe carried out if there is local autonomy all up and down theline. Interestingly, if we can believe Wright (1979), whensomething goes wrong at General Motors it is likely to bebecause the people upstairs have intervened in the processand tried to tell someone down the line how to do his job.Those of us who are highly encephalized and who canintervene in our own behavior can also testify how muchmore smoothly we move, and how much more likely we areto reach our goals, if we don't.

My main complaint with the book was that it was far tooshort; it did not tell me nearly as much as I wanted to knowabout many topics. Time and again, just as I thought I wasgoing to find an answer to some question that had been stirredup, the section or the chapter would end. It is clear that agreat deal of work remains to be done, and that Gallistel haspointed the way to much of this work. I will note just twofurther topics that I think need much more examination.

Motivation tends to be regarded as an inner phenomenon;surely the total switch of programs, or dispositions, that occurswhen the animal suddenly becomes frightened or graduallybecomes hungry must take place upstairs. But there is alsolocal autonomy in motivation. Thus, while the general knowswhy the soldier is marching down the road (better than thesoldier knows), only the soldier knows why he is smoking a

cigarette. We have to think of motivation in the small as wellas on a global or programmatic scale. Local control can beseen in the sequencing of movements. Thus, as the lad runs upto the soccer ball, we can see his intention to kick it. The bodytilts back, and he takes the short step just as he approaches it.The inner sequence is: run up and kick it; the outer sequenceincludes a moment of intricately interwoven and overlappingmotor coordinations.

Gallistel has emphasized the important servo type ofcorrection mechanism. But there is another, and just asimportant, kind of correction or compensation device.Consider this: when a man raises his hand to hold it out infront of him, there is a compensatory tilting back of the bodyat the hips. It appears that balance is restored by another oneof those negative feedback loops. But that is not what actuallyhappens. Much of the time, at least, the tilting of the bodyprecedes the lifting of the hand. We have an anticipatory, or"feedforward" mechanism to make the correction. We haveto learn a lot more about such devices. Indeed, we have tolearn a lot more about all of this.

Independence and interactionin behavioral unitsWilliam ChappieBiological Sciences Group. University of Connecticut, Storrs, Conn. 06268

Much of the experimental work on motor systems over thelast one hundred years has been performed within a theoreti-cal framework that viewed movement as composed ofelementary unitary reflexes connected together in varyingpatterns. Gallistel's The organization of action represents anambitious and partially successful attempt to update ournotions about the way in which animal movements aregenerated by nervous systems. This is a good book, thoughtfuland challenging in its attempt to come to grips with thecentral problems of movement. It does not represent a newtheory, but rather a summary of where we are now. Yetperhaps it is a measure of the book's attempt to provide areductionist theory of movement that I found myself ques-tioning its premises at a number of points.

Reflexes, oscillators, and servomechanisms represent theelementary units of movement. These "quanta" are assem-bled into more general sets which may in turn be associatedwith other sets of quantal units in hierarchical fashion.Potentiation or depotentiation of various levels of such ahierarchy can then produce the combinations of the elemen-tary units required to generate a particular movement.Generation of movement in the external world often involves"cognitive maps" of that world. Portions of classic papers bySherrington, von Hoist, Weiss, and others are used to presentthe essential elements of this theory.

Perhaps most troubling is the notion of these elementaryunits. "Reflexes," "oscillators," and "servomechanisms" eachdescribe an extraordinarily diverse group of phenomena.Some may indeed be elementary units; others may becomposed of subunits. Is the oscillator of the scratch reflex anelementary unit evoked by locomotion as well as scratching oris it an intergral part of this reflex? Units observed in a"simplified" animal preparation may not be the same unitsemployed in the normal animal. The alphabet of a class ofmovements, therefore, may not be divided naturally intoreflexes, oscillators, and servomechanisms, but along othermore diverse lines.

There are, moreover, the difficulties of associating physio-logical units with behavioral ones. A discrete network of cells,such as the stomatogastric ganglion of lobsters, may exhibit avariety of different behaviors. Due to its nonlinear properties,a single cell may be a single physiological unit but several

620 THE BEHAVIORAL AND BRAIN SCIENCES (1981), 4)


behavioral ones, acting as an oscillator and as part of a simplereflex loop. What constitutes an element in the hierarchy maydepend upon the operations that define it. Thus, I do not wishto quarrel with Callistel's aim of constructing more generalmovements from elementary units, but simply to questionhow useful historically derived categories are in constructinga general theory of action.

A second difficulty arises from the role of hierarchy in atheory of action. It seems to me that Gallistel has minimizedthe difficulties surrounding hierarchy. The existence of exten-sive interactions, both behavioral and physiological, betweenrelated but separable movements is found in many systems,from eye movements to locomotion. Gallistel himself admitsthis in discussing the concept of "relative hierarchies." Is ittrue that this lability is found only at the higher levels of theaction hierarchy, or can this also be considered to be operat-ing in the interaction between pacemakers in simple systems?Doesn't the notion of a fixed hierarchy depend upon the wayin which feedback is used to control a particular movement?

But these are arguments with a book that is, after all, on theside of the angels. Simplifications are useful if they help us onour way. By assembling a reductionist theory of action,Gallistel has shown us where we are, but also how far we haveto go.

Oscillators in human motor systemsBrian CraskeDepartment of Psychology. Memorial University of Newfoundland, St.John's. Newfoundland, Canada A IB 3X9

The aspect of Professor Gallistel's book on which I want tofocus attention is that of the role of the endogenous oscillatorin motor behavior. I strongly echo his argument that psychol-ogists have in general been slow to recognize the theoreticalpower of such a mechanism, and have made little attempt toexploit its interesting properties in their models of motorbehavior. They have also been more than a little reluctant toacknowledge that there is a wealth of experimental evidencefor the existance of these mechanisms in creatures as diverseas the cat and the cockroach (Delcomyn 1980). On of themain themes in the book must be read as a critique of thosewhose thinking is wedded to the reflex as the only functionalunit of motor organization. Perhaps the time has now come,forty years after von Hoist's (1937) important paper, toexplore the modus operandi of motor behavior in man with-out the self-imposed limitation of the chained reflex. Gallistelhas reemphasized the likely importance of coupled-oscillatorcircuits as powerful and versatile components of motorsystems, and he has ably marshalled the evidence to supportsuch a view. I concur with his argument; it is this veryversatility which points to the fundamental part which suchcircuits could play in the manifold actions which characterizeso much of the behavior of higher animals.

Perhaps one of the reasons psychologists have been tardy inthe use of the oscillator concept is the virtual absence ofreadily distinguished oscillatory motor behavior in man.Although movements of a limb may be analysed to show thatthey are composed of oscillations in different planes, this doesnot show that oscillators themselves are involved in move-ment production.

It would be valuable if evidence for the presence ofrelatively long-period oscillations in humans could bepresented, for if limbs were shown to exhibit these move-ments involuntarily, then the oscillator must at least beconsidered as a potential underlying mechanism. In order toprovide empirical support for the argument concerning theexistence of the endogenous oscillator in humans, I would like

to describe some of our recent observations on motor afteref-fects. These aftereffects have been shown to be involuntary,patterned movements of limbs subsequent to treatmentconditions which may or may not involve movement, butwhich normally involve direct or patterned sequences ofeffort (Craske 1981). Investigation of motor aftereffects inthese laboratories has recently revealed a number of involun-tary oscillatory phenomena, which provide good evidence forthe presence of oscillators at a low level in the human motorsystem.

We all know of the after-contraction effect, in which asubject first presses a wrist against a wall for about twentyseconds and then steps away, after which the arm risesinvoluntarily for a few seconds and then returns to the side.This commonly accepted decription is incomplete, however;the nature of the aftereffect is in fact a prolonged oscillation.It requries only that the subject stand bending forward witharms hanging down and that large involuntary oscillations ofthe treated arm occur. These oscillations involve as primemovers both the previous agonists and the previous antago-nists; that is, the after-contraction effect is not restricted to thepreviously active muscle. The arm may sweep through 60 ormore degrees, and for different subjects the period has rangedbetween 6.2 and 159 seconds. Furthermore, despite earlierreports, the duration of the phenomenon is between 5 and 20minutes, rather than just a few seconds.

If both arms are strained simultaneously, but in orthogonaldirections, then, on cessation of strain, each arm will oscillatein the plane of its own previous effort. In this case there is atendency for the frequency and phase of both oscillations tobe strongly linked. In test conditions which follow both arms'being strained in the same direction, the aftereffects showmore independence, and the arms may move with differentamplitudes and frequencies. Duration of oscillation may alsovary, one arm coming to rest while the other continues itsinvoluntary movement.

When one arm is strained in two directions following asequence such as: forward for two seconds, brief relaxation,sideways for two seconds, and so on for twenty cycles, thenwhen the arm is allowed to move of its own volition, oscilla-tory synthesis takes place. That is, the limb describes Lissajousmovements (e.g., moves in circles or figures of eight) as thetwo orthogonal oscillations are released simultaneously andexhibit differences in the phase relationships and frequenciesof the component movements. These combinatorial motoraftereffects have been observed for the eye and tongue, aswell as the arm and leg. The fact that there is a phase shiftbetween the two components in this situation indicates thatthe temporal relationships of the treatment are in some waybeing taken into account in the release of the aftereffect,giving a hint of hierarchical organization above the morebasic oscillatory process. There higher levels of organizationmanifest themselves clearly when more complex effortfulactivities are used as treatments. For example, a subject isasked to pedal an excercise bicycle, or to shovel heavy snow orsand, or to stand on one leg and lift the other up and downwhile it is attached to a moderate weight. At the end of aboutone minute of this treatment, the subject lets the relevantlimb or limbs hang free, and allows any involuntary activityto occur; after some delay, a very slow, involuntary, approxi-mate facsimile movement will occur, showing the presence ofstrong organizational properties. In the case of the bicycle,however, the pedaling aftereffect can sometimes be in thedirection opposite to the treatment, strongly supporting theinvoluntary nature of the aftereffect. The latter observationpoints to the presence of each of the components of theoriginal action, but an absence of organization from withinthe motor system for this simpler situation. Thus oscillatorymovement of the hip and knee joint are triggered at thewrong time - that is, with abnormal phase relationships.

This brief summary of some recent observations serves, I



hope, to add some impetus to one part of the explanation ofmotor behavior espoused by Gallistel, for these data can beexplained most parsimoniously by invoking the oscillator asan underlying mechanism in human motor behavior.

The reference trajectory as anorganising principleParvati OevRehabilitative Engineering Research and Development Center, V.A. Medi-cal Center, Palo Alto, Calif. 94304

Gallistel has done a good job of putting together a complex setof concepts and synthesizing a theory of action. As generallydoes happen in such an encyclopedic work, some interestingaspects of the field fall through the cracks. One such interest-ing aspect is the generation and control of transient move-ments. The history of the movement field has shown us thebasic nature of the reflex, the servomechanism, and theoscillator as organising principles. Transient movements, suchas reaching and turning to a stimulus, appear to be prepro-grammed rather than servo-operated, and do not seem to usethe reflex or the oscillator as their basic unit. What are theorganising principles underlying transient movements?

Is Fourier theory, as suggested by Gallistel, a possibleorganising principle? In the strict sense, any time signal, suchas joint position during movement, can be decomposed into asum of sinusoids, the Fourier components. Though this maybe an economical description for a periodic movement, for atransient movement the set of frequencies or Fourier compo-nents is infinite. Therefore, there is no simplification of thecontrol problem if one attempts to generate the Fouriercomponents rather than the time signal of the movementitself.

Control of transient movement has been studied for themovement of robot arms. The desired movement of a robotarm is specified in terms of a reference trajectory, generallythe trajectory of desired joint angular velocities and specifiedintermediate and final points. Bizzi et al. (1976) haveproposed that the nervous system specifies those activitylevels in agonist and antagonist muscles that are required tomaintain the desired final position. Elasticity of muscle thenensures that the limb, or in this case the head, moves to theequilibrium position. This corresponds to specifying a refer-ence trajectory where the trajectory is a step change inreference position. Ghez & Vicario (1978) show that, in anisometric force-development task, more motor units are acti-vated during the initial phase of rapid force developmentthan when steady force is maintained. In other words, thereference trajectory may consist of two signals - an earlypulse specifying the initial rate of change of force, and amaintained value specifying the desired final force. Robinson(1973) noted that the pulse-step from the signal to the muscleswas suited to the acceleration of a mass followed by mainte-nance of a position against an elastic restoring force.

Thus one can conceive of a single movement command'sbeing translated into a set of subcommands, one specifyingthe desired final position, another specifying transient charac-teristics (such as the peak velocity, perhaps as a function ofthe level of potentiation of a motoneuronal pool), a thirdspecifying how rigid should be the adherence to the desiredtrajectory in the face of unexpected disturbances, and so on.Each of these commands may be transmitted to differentneuronal pools - the command for desired final position to apool of small motoneurons, the specification of peak velocityto a pool of large motoneurons, the command regardingtrajectory precision to neuronal pools monitoring afferent

feedback. Together these commands specify a referencetrajectory and an error criterion.

Is the reference trajectory the same as the servomecha-nism? The reference trajectory that drives the robot armgenerally operates in the servo mode, but the specification ofthe reference trajectory is based on knowledge of armmechanics. The reference trajectory in the animal also mayoperate as a servo if the error criterion is used. However,afferent feedback is not necessary for the production of atransient movement, as has been shown for head movementsin the deafferented animal (Bizzi et al. 1976). The specifica-tion of the reference trajectory itself is done open-loop,presumably based on an internal representation of limbdynamics.

Thus there appears to be the need to include, in a theory ofaction, a non-oscillator-based programming unit that canspecify the transient characteristics of a movement and thatcan drive a movement irrespective of the presence of feed-back.

Nodes, notions and neuroscienceRobert W. DotyCenter for Brain Research, University of Rochester Medical Center,Rochester. N.Y. 14642

Gallistel's book is, unequivocally, an important and creativeanalysis of the manner in which the central nervous systemcoordinates and initiates purposeful movement in creatures asdiverse as insects and primates. Most impressive is theauthor's ability to extrapolate exceedingly complex actionfrom a few underlying, relatively simple principles. Theexamples reproduced in extenso from the original literatureare well chosen and lucidly explicated, particularly the prin-ciple of the "efference copy." Gallistel's emphasis on thelattice nature of hierarchical organization in the nervoussystem is perceptive and useful.

Perhaps the major contribution will turn out to be thesuggestion that afferent activity is encoded into patternsappropriate for organized output. While no one can currentlysay what this means, it provides a reasonable guilding hypoth-esis in a field of endeavor still struggling to identify ameaningful code in the digitally transmitted representationsof sensory events. It may also provide a new insight into themanner in which the afferent portal "gates" the input intoparticular channels and thereby selects which of many reac-tions will occur to pluripotential input (Doty 1976). The"gating" is most probably based on the spatiotemporalpattern of the afferent discharge, but, in view of Gallistel'spenchant for "oscillators," it bears noting that, in one instancewhere "oscillation" and "resonance" could reaonsably havebeen expected, it was almost certainly lacking in the centralneural mechanism (Doty 1951).

The book is sometimes annoyingly pedagogical. It is hardto imagine a reader who would stay with the exposition topage 299 yet not know what an electrode is - but it is dulyexplained to him. More important than annoyance, however,this unnecessarily constrained approach limits the documen-tation of many of the facts alluded to, and the reader iscarefully spared many of the complications which subsequentresearch has uncovered - e.g., on the "myotypic response."

Although inhibition as a mechanism of coordination andcontrol is clearly identified by Gallistel, I think its impor-tance, both in restraining the operation of irrelevant synergies(Roberts 1974; Doty 1976) and in accessing motoneurons forensuing patterned activity (Doty 1976) is not sufficientlyemphasized. Indeed, Pearson and his colleagues (1980) have

622 THE BEHAVIORAL AND BRAIN SCIENCES (1981), 4)

Commentary/GaWisteh Organization of action

now elegantly detailed the manner in which visual inputcauses a grasshopper to jump; and inhibition is a crucialfactor!

As Gallistel's discussion wanders farther from neurophysio-logical principles one gets sentences like the following: "Theassumption that food nodes on the animal's cognitive mapsare likewise connected to this hunger center means that apotentiating signal from the hunger center is automaticallyconducted to nodes representing food" (p. 352). To his credit,Callistel recognizes this as merely nominalizing a problem;yet this is how Weiss and Skinner "went wrong" - by simplyverbalizing, describing, or hypothesizing processes withoutreference to their neurophysiological likelihood. On the otherhand, one must eschew pretense at understanding that whichremains basically mysterious. The "nodes," the (digitalized)Fourier transforms, and the preferential "potentiations"carry, in essence, no more explanatory power than the "ho-munculus," or the "psychical" activity of which Sherringtonwrote so poetically, and which Callistel so uncategoricallydiscredits. Forthright identification of the limits of knowl-edge is an essential feature of its expansion - no Copernicus solong as all epicycles are believed to turn in perfect coordina-tion. The ultimate understanding of the "organizaiton ofaction" must include mnemonic and conscious contributions,and, for what is presently known about the nature of theseprocesses, the critical feature of either "homunculus" or"node" is the profession of ignorance. Callistel confesses thathe has a certain "feeling" when his cognitive map comes intocongruence with reality. One wonders whether the wasp doeslikewise - an idle question, were one not able to hope forelucidation of the underlying neural processes in each case(Doty 1975; Bartlett & Doty 1980).

Network foci in integrated action: Units orsomething else?John C. FentressDepartment of Psychology, Dalhousie University. Halifax, Nova Scota B3H4J1

As Callistel emphasizes throughout his valuable text, a majorchallenge to the behavioral and brain sciences is to examinethe network of events that (a) permit the organism to articu-late distinguishable actions and (b) mold these actionstogether into functionally coherent ensembles. In addition, asthe author emphasizes, it is essential to seek rules by whichthe various "levels" of integrated performance (e.g., move-ment and motivation) may be conceptually joined together -a task that I too have been especially concerned with in recentyears (Fentress 1976; 1980; in press). Callistel has understand-ably chosen to base his arguments on a unit-structure modelof behavior and the hierarchical arrangement of these sepa-rately defined units. It is upon these points that I focus mycomments.

What is a unit of behavior? Dictionary definitions of theterm "unit" lead us to anticipate a structure that is (a)indivisible, (b) separate, and (c) stable. It is useful to exploreeach of these attributes further.

1. Are behavioral units Indivisible (I.e., unitary)? Thisdepends upon how and where we look. My own work onrodent grooming, to which Callistel kindly refers, shows thatindividually defined "actions" have a statistical, but notcertain, association to one another in time. It is, for example,possible to perturb some features of grooming while leavingthe others quite unaffected; i.e., the grooming unit is subdi-visible in its rules of expression. At a higher level of organiza-tion Hinde (1959) noted some years ago that motivationalcategories ("drives") can be fractionated - e.g., certaincomponents of feeling or fighting or mating can be selec-

tively altered. More recently, at a more restricted level ofanalysis, a number of workers have shown that even relativelysimple motor acts (such as scratching in turtles; Stein &Grossman 1980) can often be fractionated (e.g., into incom-plete cycles plus variations of muscular action from one cycleto the next). Similarly, Colani (1976) demonstrates how aparticular action in mammals can be performed reliablythrough a variety of kinematic articulations. The unitarynature of "units," whether defined at motivational or atmotor levels, is thus, at best, a useful approximation.

2. Are behavioral units separable (I.e., Independent)? Theforce of this question was first brought home to me when Ifound that a variety of independently defined motivationalsystems (e.g., "fear" or "exploration") could facilitate, as wellas block, rodent grooming actions - partially as a function ofthe degree to which these apparently unrelated systems wereactivated (e.g., Fentress 1976). It was brought home a secondtime when I found that the detailed form of an individualgrooming stroke could be influenced by its neighbors (Fen-tress 1976; 1980; in press), a phenomenon not that differentformally from issues of coarticulation and perception of the"segments" of human speech (e.g., Studdert-Kennedy 1976;Liberman 1980). A third lesson came to me from the elegantdescriptive study by Woolridge (1975) on grooming patternsin mice. His detailed measures of area of the face covered bythe paws, velocity of individual movements, etc. duringmouse grooming sequences all seemed to reflect a continuousdistribution of processes that crossed over the categories ofaction that I had previously proposed (e.g., Fentress 1972). Afinal example can be seen in the conceptually importantunpublished dissertation by Bellman (1979), who showed thatindividual features of feeding and fighting in lizards may beblended, given the appropriate circumstances. In short,"units" of action, as we define them today, are not immutableor fully separable, but can vary within limits, and evenoverlap, in ways not yet fully understood - but in some senseas a function of the broader surroundings within which they,as individually defined, occur.

3. Are behavioral units fixed (I.e., static)? It wouldcertainly be nice if they were, but I doubt whether this will befound to be the case. Behavior, after all, is fundamentally anested set of more or less coherent processes, not a set of"things" in any strict sense. Let us take the idea of centralpattern generators (which Callistel reviews admirably) as anexample. By now we should expect that pattern generatorsare neither unitary entities nor necessarily independent, in astrict sense, from their surround (e.g., Selverston 1980, andaccompanying commentaries). The only points I wish toemphasize here are that the balance between central regula-tion and sensory influence can vary systematically as afunction of movement, speed, etc., and that even the specific-ity we assign to a behavioral control system need not be fixed.Thus, Woolridge and I have recently found (unpublished)that the degree of influence of specified extrinsic factors uponthe patterning of grooming actions in mice can shift systemat-ically with the speed at which these movements areperformed (cf. Fentress 1980) - as if "the central program"became more autonomous from the periphery when it wasstrongly activated. This implies that the boundaries of controlprocesses in any given form of behavior (i.e., the definingcharacteristics of a "unit") are modifiable, but in a rule-givenway. Analogously, the "breadth" (specificity) of controlboundaries that participate in grooming and a variety ofother specifically defined actions can vary systematically as afunction of stimulus-strength, time over which a set of stimulioperate, etc. Many other examples could be given if spacelimitations permitted.

Toward a view of coherent processes as an alternative tounit structure. So, what does all this mean with respect toGallistel's helpful attempt at providing us with a synthesis of


Commentary/GaMisteh Organization of action

integrated action? I think it means that our definitions of"units" of behavior must be rethought. I think it means thatunits are, to borrow from Sherrington (as quoted by Gallistel),"a convenient . . . fiction" - useful, within limits, until some-thing better comes along.

And what form will this "something better" take? Here Ican only speculate, though I do so with reason. It will take,first, an explicit awareness that integrated behavior is a nestedset of more or less coherent processes rather than a set ofindivisible, independent, and separate things. It will take anincreased appreciation for the rules of relation amongstseparately defined processes as a key to understanding (in adeeper sense) these processes rather than merely the reverse(i.e., the assemblage of individual processes to constructhigher orders of organization). That is, it will take animproved awareness amongst the neurobiological communitythat change and relation are key ingredients in their enter-prise.

A brief illustration here may help make the point. Onebasic feature of many action systems is that the subprocessesof movement may be varied over a wide range while coher-ence at a higher level is maintained — I can brush my teeth bymoving my arm or my head, or innumerable combinations ofthe two; a mouse can make sweeping contact with one part ofits face through a variety of kinematic combinations ofadjacent limb segments, head and forelimb movements, etc.Coherent processes at one level - either "higher" or "lower" -may be reflected in variations at another. One thus frequentlyobserves what I have previously called relational constanciesin behavior, where coherences in "higher levels" of expression(toothbrush bristles passing over the teeth) are maintainedthrough complex variations at "lower levels" of expression(individually defined limb movements; cf. Golani 1976). It isnot one level versus another, but some synthesis among themthat can itself vary in time.

In some respects, as Gallistel emphasizes, future researchwill need to exhibit an increase awareness of problems inrelating hierarchically distinguished levels of behavioral(and/or brain) organization. I do not think, however, that itwill simply be a case of the foci of network actions beingexamined at a variety of levels of order, or of one being usedto explain another (cf. Rose 1981). One can but hope thateach of these levels will contribute something of significanceto its neighbors - not as "units," but as more or less coherentprocesses in their own right. This is my own extrapolation ofthe important message of Gallistel's book. While I mightappear to quibble with him on certain details of exposition -especially his treatment of "units" and unidirectional "hierar-chies" - I applaud his efforts to lead us toward a moreintegrated appraisal of integrated function than was other-wise readily available.

Summary. So, let me summarize briefly: "Units" of behav-ioral action are sometimes convenient fictions. They providea clear format for distinguishing one feature of behavior fromanother, a task, as Uttal (1978) notes, that is much moredifficult than is the separation, say, of one anatomical (e.g.,brain) locus from another. Behavioral "loci" must take intoaccount not only that behavior is multilayered, but that ateach layer behavior involves constructs of change (i.e.,process), and that both between and within layers there are amultiplicity of nonfixed relations. What we are left with,then, is the search for foci in both the expression and thecontrol of integrated action in a manner that is appropriatelyfluid as well as multilayered in its content. Models that aretruly dynamic, relational, and multilayered will, in thefuture, I suspect, make unit-structure and linear-hierarchyconceptions of behavioral and brain science seem as unsatisfy-ing as are static, isolated, and linearly ordered mechanicalconcepts when viewed in the context of modern physics (e.g.,Bohm 1969).

"A new synthesis?"

Sten GrillnerDepartment of Physiology III. Karolinska Institutet, S-114 33 Stockholm,Sweden

Gallistel's The organization of action: A new synthesis is forthe most part enjoyable reading. To illustrate well-estab-lished, even if not always well-known, findings, Gallistel haschosen to print full papers or parts thereof (45% of the text inthe book) from the works of Sherrinton, von Hoist, D. Wilson,Fraenkel, and Weiss. These classic papers are provided withcomments relating them to more recent findings. In this wayGallistel deals with the Sherringtonian reflex concept,coupled oscillators, servomechanisms and efference copy, andhierarchical organization of movement control - which are allplaced in relation to animal behaviour - for instance, centralmotive states. He arrives at a very general picture of differentaspects of movement control (action) that, as far as I can tell,is not in the least different from the one that most of mycolleagues in my own field have had for years, and that hasguided much of the work in this field at least throughout theseventies. There is nothing scientifically new in this book. It istherefore difficult to provide a commentary on what ispresumed to be "a new synthesis." Part of this field has been asubject of discussion in some depth in prior BBS target articlesby Selverston (1980) and Kupfermann & Weiss (1978).

What is new is that a physiological psychologist, active incircles with little knowledge about the neural control ofmovement, has taken the trouble to go through this literature.He has been pleasantly surprised to find that in fact a greatdeal is known. He has therefore written a book to inform hiscolleagues and students about his new treasure. This is all verygood, and by reading this book many researchers maycertainly add to their perspectives. To call the book "a newsynthesis" is, however, not only presumptuous, but in factscientifically misleading. One might suspect that the title wasimposed on the author just to improve the sales of the book (Ibought the book for that reason myself), but this does notappear to be the case on the basis of what Gallistel himselfwrites about his conceptualization. (The same unfortunatelyappears to apply to another "action theorist," Turvey 1977.)

The book reads well, and I did not discover any majorerrors. It takes examples from a limited group of motor acts,frequently locomotion, in a variety of animals. To my mind itwould seem essential at least to go through all the main typesof movements in a systematic and penetrating fashion ratherthan to extrapolate from a few examples. It is clearly toomuch to ask to expect that the author know this wideliterature well, since he is not in the field. Therefore it mustbe accepted that quotations, references, and examples willseem rather arbitrary and the account of different phenom-ena sometimes superficial.

What I have just said may seem harsh. I would like to add,however, that is is a most admirable feat to write this book on"action" (motor control) from the outside in order to bringknowledge of principles of motor control to the field ofcognitive psychology. We are now in an exciting era when theboundaries between different neurobiological and psycholog-ical disciplines break down. This book is a manifestation ofthis trend: what can be more important than to unite cogni-tive psychology with basic neurobiology? This was expressedby von Hoist in the following way: "It is hoped that thisarticle will contribute to the gradual disappearance ofattempts to describe the functions of the highest developedorgan of the body with a few primitive expressions. Thesooner we recognize the fact that the complex higher func-tional Gestalts which leave the reflex physiologist dumb-founded in fact send roots down to the simplest basalfunctions of the CNS, the sooner we shall see that the



previously terminologically insurmountable barrier betweenthe lower levels of neurophysiology and higher behavioraltheory simply dissolves away" (von Hoist Mittelstaedt 1950,and p. 209 in Gallistel 1980).

What I would like to see, however, is a new book byGallistel or somebody of his calibre, on the same generaltheme, provided that he had specialized coauthors for each ofthe chapters who could provide the necessary precision andnuances for all statements made. Such a book could become amajor contribution to science. The present book is useful as anintroductory text for graduate students.

Hierarchy and behaviorJerry A. HoganDepartment of Psychology. University of Toronto, Toronto, Ontario, CanadaM5S 1A1

The organization of action is an interesting, intelligentlywritten, stimulating, and provocative book. It is interestingbecause of its format. It reprints, in whole or in part, sixclassical papers on the neurophysiological mechanismsunderlying action patterns. Gallistel precedes or follows eachpaper with commentary, and then integrates this materialinto a theory of how action is organized. The book is intelli-gent because the choice of papers is so clever that the reader isalmost forced to embrace the theory before it is formulated. Itis stimulating because the original papers as well as Gallistel'sown contributions sparkle with the enthusiasm inherent inpresenting good ideas that are well supported. And it isprovocative because some of Gallistel's speculations, in chap-ters 11 and 12, about how cognitive preocesses control actionare truly outrageous.

The goal of the book is to discover the units out of whichaction is formed and the principle by which the units areintegrated. The units turn out to be reflexes, oscillators, andservomechanisms, and the organizing principle is the hierar-chy. In very important ways, Gallistel's theory of action issimilar to Tinbergen's (1951) familiar hierarchical organiza-tion of instincts. Tinbergen's formulation was based on manyof the same papers reprinted in The organization of action,so the similarity should not be surprising. What Gallistel hasadded is a more extensive discussion of the units themselves, amore satisfactory foundation of the theory in the facts ofneurophysiology, and an extension of the theory to the realmof cognition.

I shall comment on two closely related aspects of the basictheory in which I think some confusion exists: levels ofanalysis and hierarchical structure. Let me begin with theproblem of hierarchy.

Gallistel's argument for a hierarchical organization ofaction begins with the hierarchical system proposed by PaulWeiss (1941, partially reprinted in chap. 8). This systemrecognizes six levels of motor organization: (1) movement ofmuscle fibers controlled by a single motor neuron; (2) move-ment of a whole muscle; (3) movement of a single joint; (4)movement of a whole limb; (5) a locomotor act such aswalking, jumping, or swimming; and (6) motor acts in "theservice of the animal as a whole under the control of thesensory apparatus." Gallistel than proceeds to subdivideWeiss's level 6 into yet more levels. At least two such levelsseem well supported: the level of the complex motor act(fixed action pattern) and the level of functional integrationof motor acts (behavioral or motivational systems such ashunger, aggression, and sex).

Now, throughout his discussion Gallistel implies (as doesTinbergen 1951, Fig. 98, p. 125) that this hierarchical schemereflects "the organization of the underlying neurophysiologyand neuroanatomy" (p. 292). Here, I think, is where theconfusion arises. Dawkins (1976), in a recent descussion of

hierarchical organization, calls attention to a distinctionbetween hierarchies of connection and hierarchies of classifi-cation or embedment. In a hierarchy of connection, superiorelements exert control over inferior elements in the same wayin which a captain gives orders to a lieutenant. In a hierarchyof classification or embedment, inferior elements are actuallya part of superior elements in the same way in which aplatoon is part of a company. Platoons and companies aredifferent classifications of the same elements: soldiers.

If we apply this distinction to Gallistel's hierarchy, we seeimmediately that at least the first five levels posited by Weissare a hierarchy of classification With respect to neuralconnections, these five levels are in fact at the same level - thelevel of the primary motor neuron or "final common path" ofSherrington. The primary motor neurons are of course inter-connected and are subject to mechanisms such as reciprocalinhibition, but there is no evidence to suggest that theseinterconnections are hierarchically organized. Actually,Weiss's whole system is a hierarchy of classification in whichbehavior in the service of the animal as a whole is logically thehighest level of organization: Weiss never implied a connec-tive hierarchy of the sort Gallistel attempts to construct.

In a sense, Gallistel does recognize this distinction, becausehe finds it necessary to postulate "intermediate units oforganization" (p. 288). Intermediate units have a degree ofcomplexity that would put them at about level 5 in Weiss'ssystem. I would argue that these intermediate units are thelowest level of behavioral organization in terms of a neuralhierarchy, and that Weiss's lower levels are merely embeddedin these units.

Once we ascend from the level of an intermediate unit, Ithink, the evidence for hierarchical neural organization isunassailable. Gallistel's presentation and discussion of theevidence are clear, concise, and convincing. It is perhapsworth mentioning, however, that hierarchically organizedbehavior systems are not the only way to activate motorneurons. There are several parallel routes, including thewell-known pyramidal cells from the motor cortex. It seemscertain that these motor-cortex cells are not generally con-trolled by diencephalic neurons. Such influences fromdifferent parts of the nervous system can be superimposed atthe level of the primary motor neuron, but are not themselvespart of the behavior-system hierarchy.

Finally, let me mention the problem of levels of analysis.My point here is implicit in what I have just said aboutintermediate units. It may be possible to describe the basicelements out of which action is organized as reflexes, oscilla-tors, and servomechanisms. But even the simplest spinalreflex involves coordinated movement of a whole limb, andsingle oscillators are postulated to control movements ofwhole fins in fish by von Hoist (1937) and of whole legs ininsects by Wilson (1966). Thus, these elements have a degreeof complexity somewhere about Weiss's (1941) level 5. Orga-nization of action at a lower degree of complexity may not bebehaviorally meaningful.

In conclusion, I think Gallistel has done an excellent job ofpresenting a theory of action in a stimulating and provocativeway. Consideration of the sorts of points I have made shouldpique discussion that may lead to clarification and refinementof the basic theory.

Effective procedures versus elementaryunits of behaviorJohn M. HollerbachArtificial Intelligence Laboratory, Massachusetts Institute of Technology,Cambridge, Mass. 02139

The main thrust of Gallistel's The organization of action is a


Commentary/GaUisteh Organization of action

broad attack on dualism as it pertains to the control ofmovement. By proposing specific mechanisms which canrealize intentions, the author seeks to bridge the gap betweencognitive intention and the actual production of movement.The author is addressing his arguments both to physiologistsand to cognitive psychologists, with the ultimate hope ofshowing that some of the distinctions between the fields areonly apparent, not real. Be defining cognition as the domainof mental representations, the author shows that even thelowly wasp must have cognitive abilities, due to its terrain-matching abilities.

Without actually coming out and saying it, the author isusing a well-known thesis in the theory of computation tojustify the attempt to emody mentalist functions in physicallyrealizable neural circuits. Church's thesis states that anythingwhich can be formulated as an effective procedure can becomputed by a Turing machine. Basically, what the thesis issaying is that any idea which can be described in sufficientdetail can be physically realized. Church's thesis, it must beemphasized, is a hypothesis and not a proof. Nevertheless, thealternative is not palatable, as it takes us into the realm ofmysticism, because there would be mental processes whichwe could not know and could not describe.

Another line of thinking which supports the author's mainthrust is the recognition that the central nervous system (CNS)had to evolve in the context of controlling its physicalmachinery. Animals have been propelling masses under theinfluence of gravity for eons, and somehow a representationof effective control of limbs must have worked its way intothe CNS.

The structure of the book is a series of introductions anddiscussions centered around excerpts from classic papers inmotor control. The author emphasizes that he doesn't want abook of the latest word, and that the student of motor controlis best advised to read classic papers. It is, of course, theauthor's prerogative to structure his book as he sees fit, but itis my opinion that this structure does not always facilitate theprofessed goal of convincing psychologists of the potential forphysical embodiment of mental processes. Through thechoice of such classic papers, the book takes on the tone of ahistory of ideas concerning the evolution of motor control.This tone sometimes interferes with the professed goalbecause the author must spend a great deal of time updatingor disavowing some of the older ideas. Despite the author'sreluctance to include the "latest word," I feel it would havebeen more forceful to start from the most current thinkingabout some of these motor-control ideas.

The author has identified three principles which hebelieves are among the fundamental building blocks of move-ment - namely reflexes, servomechanisms, and oscillators.Moreover, he argues for a hierarchical structure for motorcontrol, a paradigm used to describe many other aspects ofCNS organization and hence readily acceptable to psycholo-gists. The trump card for showing how intention can belinked to action is selective potentiation, which operates onthe hierarchical motor-control structures. The papers theauthor has chosen provide experimental evidence to supporthis proposals.

My main criticism of this choice of principles of motorcontrol is probably one the author would readily agree to, butone which should be stated anyhow. These principles arecoarse descriptions of some aspects of motor behavior, and arenot detailed enough and probably not rich enough to consti-tute effective procedures for motor-control functions. Thedifficult question of what is an elementary unit of behaviorcannot be answered yet, and it may be that the question is illposed.

The author has the greatest difficulty in making the reflexan effective concept. What makes a reflex particularlyawkward for the author is that Sherrington was a dualist. Theconcept of a nervous system reacting to the world rather than

acting spontaneously is anathema to the notion of a centralrepresentation. By the time the author has circumscribedsome of Sherrington's ideas such as chaining and a refractoryperiod, and by the time he has described how the centralnervous system can modulate reflex response, one is leftwondering what the concept of reflex really means.

The author seems to be incorporating more central-nervous-system activity into the concept of reflexes than isnormally accepted. The role of reflex activity in the control ofmovement is a controversial and ongoing subject of research,and it is probably premature to elevate reflex activity to therole of a fundamental building block without further under-standing of the nature of its contribution to motor control. Infact, many recent experiments on load compensation duringarm movement in primates indicate that the gain of the spinalreflex is very low and that long-loop activity via the brainstemand higher centers provides by far the greatest part of loadcompensation. Some workers call this activity long-loopreflexes, but in so doing the term "reflex" has become just alabel which doesn't provide any insight.

Sherrington, of course, made significant contributions atthe cellular level of understanding. Callistel also makes apoint of diagramming specific neural circuits that couldimplement some of the processes he is illustrating, with anopen admission of the potential problems this could lead to.The zeal to prove that intelligent processes can have aphysical embodiment leads to the potential problem that toostrong a concentration on the cellular level may miss the pointof the computation. Since the author is not averse to usingcomputer metaphors, focusing on cells is like trying to under-stand how a computer program works by measuring transistoroutputs. Naturally the analogy to computers must betempered with the knowledge that there is more locality toneural circuitry than there is to computer circuitry and thatcells may be carrying out a higher level computation thantransistors. Nevertheless, the recurrent inhibition networkdiscussed by the author sounds like an XOR gate. An XORgate is a fundamental logic unit in a digital circuit, but in andof itself it implies nothing about its use.

Fourier theories of visual image processing and of auditoryprocessing of speech, for both biological and computer-basedsystems, have been common. It was inevitable that someonewould propose a Fourier representation of motor commands.Fourier representations have proven to be bad ideas in visionand audition, and it is distressing to see history starting torepeat itself now in motor control. A Fourier decompositionof a signal is often merely an exercise in curve fitting, and thecurve fitting does not necessarily capture the essence of thesignal structure.

The term "servomechanism" is borrowed from controltheory, where the meaning of this term is fairly definite. Aservomechanism comprises a reference signal, a sensor fordetecting the amount of error between the reference signaland the actual state of the device, and a feedback law which isused to synthesize new control signals based on the degree oferror. This concept can be broadly applied as a paradigm tomany motor activities, since animals often pursue some goaland modify their actions if they start to drift from the goal.Once again, however, there are problems in broadening amore specific concept.

It is important to attempt to distinguish servomechanismsfrom adaptive controllers. The more logic that is involved inresponding to an error signal, the more a controller becomesan adaptive one and less a servomechanism. In talking aboutwasp flight on page 148, the author remarks that the wasptaxis involves perceptual mechanisms of a high order as wellas a memory. When there is this much logic involved in errorcorrection, it is not clear what the ultimate error signal is, orhow it is processed.

Another problem with the servomechanism concept is thenormally slow speed of conduction of nerve impulses relative



to the speed of movement. Control theory tells us thatservomechanisms based on error signals with significantdelays will result in unstable systems. Intuitively, if it takes along time to process an error signal and devise a correctiveresponse, then by the time the response is operative thesystem will already have moved to a new state for which theresponse is inappropriate. The muscle spindle system wouldappear to be an obvious candidate for part of a servomecha-nism. However, long-loop delays from muscle to highercenters and back are on the order of 70-100 milliseconds,which, at least for the more rapid movements, is too slow toact as a servomechanism.

Recent trends in motor-control research emphasize feed-forward planning rather than feedback correction. Posturaladjustments, particularly in locomotion, are made beforemovement commences or contact with the environmentoccurs. On page 138 the author explains how a servomecha-nism might interact with an oscillator for terrain adaptationduring locomotion of insects. In higher animals, at least,terrain adaptation appears to have a greater cognitive orfeedforward component: there is active anticipation going on.[See also Roland: "Sensory Feedback to the Cerebral CortexDuring Voluntary Movement in Man" BBS 1 (1) 1978.]

The role of proprioceptors in the control of movement is infact quite puzzling. The more obvious hypotheses about theuse of muscle spindles, Golgi tendon organs, and joint recep-tors, such as the servomechanism hypothesis, do not appear tohold. As good a guess as any at the present time is thatproprioceptors signal unusually large deviations fromintended movement, and that higher centers use this informa-tion to devise rather gross corrective movements.

Along the line of differences in control systems betweeninsects and higher animals, I feel the author should havedirectly addressed a point raised by Weiss (1941) on page 234.This point is that the higher the animal on the evolutionaryscale, the more independent a control of joints and muscula-ture it has. Consequently the type of control strucutre formovement may change along the phylogenetic scale.

Anatomical and physiological observations strongly suggestsome sort of hierarchical motor-control organization, as advo-cated in the excerpt from Weiss. The author modifies thenotion of a strict hierarchy to a lattice hierarchy. In the limit,a latticed hierarchy becomes a heterarchy, where the conceptof level disappears and every module may freely interactwith every other module.

Selective potentiation acting on a latticed hierarchy proba-bly has the effect of turning the hierarchy into a heterarchy.The author makes much of the ability to set a generaltendency through selective potentiation, which can result in ageneral course of action without a detailed specification ofthe steps needed to achieve the action. Setting activationthresholds for modules of a hierarchy and allowing interac-tions with the environment or other modules to triggeractivation of a module is a well-known concept in the artificalintelligence (AI) field, where this sort of control structure isvariously named production systems, daemons, actors, etc.This control structure is essentially heterarchical because theinteractions between the modules are ill defined and aresubject to local recognition of a pattern which results inactivation of the module.

Hierarchical versus heterarchical organization of controlwas a hotly debated issue ten years ago in AI. Eventually thisissue was abandoned because the concepts of hierarchy andheterarchy were considered too simplistic to explain complexintelligent processes. To be sure, there are aspects of theseprocesses which seem approximately hierarchical or heterar-chical, but this is too rough a cut. Instead of applying suchglobal paradigms as hierarchy, researchers in AI have focusedon more specific problems such as language parsing or low-level vision and have let the requirements and constraints ofsolutions to a specific problem dictate the nature of the

control structure. What usually emerges is a rich and uniquecontrol structure specific to the problem, and this controlstructure goes far beyond concepts such as hierarchy.

In conclusion, the main concepts advocated in this bookhave had a historical impact on molding thinking aboutmotor control, and this book is a useful history of theevolution of these concepts. The attempt at bridging the gapbetween physiology and psychology and at counteractingmentalist philosophies has been convincing. Whether theseconcepts constitute elementary units of behavior or controlstructure is, however, problematic, because the concepts aresometimes not clearly defined or are coarse descriptions ofmuch more complex processes. Von Hoist's words on page209 provide a fitting summation: "It is hoped that this articlewill contribute to the gradual disappearance of attempts todescribe the functions of the highest developed organ of thebody with a few primitive expressions."

Gems set into a base matrixRudolf JanderDivision of Biological Sciences, University of Kansas, Lawrence, Kans.66045

Surely a new synthesis of how action is organized is what wedesperately need. How promising is the title of Gallistel'sbook, and how thoroughly disappointing the text, whenapproached with the above expectation. Indeed, the book is"plagiarism on a grand scale," as the preface's first sentenceapologetically admits; and thereafter one discovers that muchof the text merely consists of reprints, albeit well-selectedearly gems. These are then set into a matrix of the author'sown concepts and theories, which together constitute thebook's original component, which will be scrutinized in therest of this commentary.

Given the blatant mismatch between title and text, doubtsabout single authorship of the two seem at first to be justified.However, after one finds how riddled with inconsistencies theoriginal text is, this hypothesis becomes untenable. Sinceexposing and correcting all the flaws of logic and argumenta-tion would amount to writing a whole new book, I insteadpick out a few representative examples, first at the concep-tual, then at the propositional level.

Gallistel's logical starting point for his line of reasoning isSherrington's idea that all complex behaviors can be decom-posed into elementary units of behavior. Note that "elemen-tary units of action" would better fit the context because thisterm appropriately excludes the behavioral-input side:sensory reception, perception, and cognition. After this minorblemish the conceptual muddle keeps building up, step bystep. Without supporting reasons we are told that there arejust three important types of elementary behavioral units; toSherrington's one original type, the reflex, the author adds theoscillator, his only genuine elementary unit of action, and theservomechanism, which is rather a unit of behavior than aunit of action. These inconsistencies are topped by violatingvirtually all logical rules for constructing a scientificallyuseful categorical system.

Thus, and most importantly, the elementary classifyingconcepts are neither mutually exclusive nor exhaustive, asthey certainly should be. Notice that no objective criterion tospeak of is given for drawing the line between reflexes andservomechanisms. Virtually all reflexes, as is well known, arethemselves servomechanisms, or at least components ofservomechanisms. In order to escape from this artificiallycreated conceptual dilemma nothing but a subjective solutionis offered: the reflex - as compared to a servomechanism - isa servomechanism whose feedback component is (arbi-trarily?) not considered (p. 11).



A servomechanism, in turn, is defined so loosely that thissupposedly elementary term correctly applies to countlessdefinitely nonunitary behaviors such as overall feedingbehavior. Finally, from among all the diverse, intrinsicallydriven, elementary movements only the oscillator type isconsidered important, without any reason being given, and allthe nonrhythmic action types go unmentioned. Altogether,with all the crucial rules for setting up a set of classifyingconcepts being violated, I cannot imagine how anyone couldsucceed in understanding the organization of action patternsby employing such an unscientific terminology.

If the exasperated reader tries to infer the meaning of thethree elementary concepts from their use, he has to sufferfurther frustration. A case in point: a scratch reflex, by thedefinition of a reflex, should be an atomic behavioral unit.Nevertheless, this unit contains as one of its constituents a trueoscillator which, by definition, is an atomic behavioral unit initself. Adding to this muddle is the ambiguous use of "oscilla-tor" as, on the one hand, merely a nervous mechanismgenerating rhythmic output and, on the other, as a unit ofbehavior comprising both nervous and muscular processes.Similarly, there is no way of understanding why the compos-ite complex behavior pattern of a taxis is at one pointconsidered an elementary behavioral unit, a servomechanism(pp. 143, 402), and at another point a more complex multiunitbehavior (p. 275).

If, finally, the utterly desperate reader seeks help from theglossary, his conceptual confusion will be furthercompounded. There the elementary unit of behavior isparaphrased as "a nerve and muscle circuit capable by itselfof mediating a simple naturally occurring movement." Thus,strangely enough, reflexes and servomechanisms are nowruled out as units of action by virtue of their constituents,which are not only nerves and muscles but definitely alsoreceptors.

As the only viable solution to this plight I suggest thatsensory reception, perception, and cognition be disregardedwhen one is building a hierarchic system of concepts todescribe action patterns. Gallistel's much more ambitiousattempt at developing a comprehensive system of neurophys-iologically explanatory concepts for action patterns is boundto fail given our current state of pertinent ignorance. Moreconcretely, what I have in mind is some psychobiologicalgeneralized analogue for the enviably concise and expedientsystem of the psycholinguist: phoneme, morpheme, word,phrase, sentence, discourse.

At the theoretical (model-building) level, too, blatant viola-tions of epistemological principles abound. Again, only a fewinstances can be discussed. Take the newly proposed notion ofthe lattice hierarchy, with its superimposed informationalflow or command systems (Fig. 3.1 and Fig. 1 of Precis on p.52). If such subsystems all act at once, as is assumed in theproposed theory, then the motor output can be nothing but adysfunctional mishmash. As this is normally not the case inbehavioral reality, this fact falsifies the theory. Long agoethologists identified this very problem and proposed andsubstantiated the existence of mutual inhibition betweencompeting subsystems as a simple, powerful, and efficientmechanism ensuring mutual exclusion between biologicallyincompatible sets of behavior (e.g., Iersel & Bol 1958). Ignor-ing this necessary and time-honored ethological theory inproposing the lattice hierarchy as an explanatory principle isa deplorable step backward in the understanding of howaction is organized.

Whereas there is little concern about whether the proposedlattice hierarchy works (i.e., is capable of generating anoutput pattern resembling real action), workability is theoverriding criterion in support of the proposed Fouriermodel, which is supposed to explain the generation of anyaction pattern, no matter how complex (p. 370 ff). In theauthor's assessment of this model, the importance of contrary

facts pales in comparison to workability; even negative datamentioned at other points in the book are ignored, forexample, nonlinear summation (p. 41 ff.) and the magneteffect (p. 99 ff.). My main argument in this context would bethat if some behavioral pattern is realized, this is in itselfsufficient and necessary to show that the underlying mecha-nism truly works; a falsified theory does not add a jot to thisstraightforward conclusion.

Similarly, what could be the justification for rediscussingDeutsch's workable but hardly supportable theory of mentalmaps? (p. 350 ff.) Among the decisively falsifying facts it issufficient to mention that some spiders, ants, honeybees, andrats are known to be capable of preplanning novel shortcutsbased solely on detour experience, and hence by means ofmental maps that do not match Deutsch's theory (Gorner1958; v. Frisch 1967; Jander 1957; Tolman, Ritchie, & Kalish1946).

Nobody who is sufficiently informed will disagree withGallistel's well-taken central point that the study of actionpatterns is seriously underrepresented in contemporarypsychological teaching and research. One strangely humanexplanation for this relative neglect is the psychologist's longtradition of ignoring or even rejecting ethological theoriesand knowledge. As an interesting historical fact, I would liketo mention that in 1954 E. v. Hoist (who figures so promi-nently in this book) joined with K. Lorenz, the "father ofmodern ethology," in founding the renowned Max-PlanckInstitut f iir Verhaltensphysiologie.

Overall, I wish this book had been offered merely asselected readings of classic papers on the organization ofaction patterns. At present, a new, true psychobiologicalsynthesis of the organization of action is nowhere visible.

Input-output relations ingoal-directed actionsM.JeannerodLaboratoire do Neuropsychologie Experimentale, INSERM Unite 94, 69500Bron, France

I felt quite in harmony with many of Gallistel's conceptionswhile reading his book. There is, however, one importantaspect of the organization of action which I think he hasoverlooked. To my understanding, the motor system, even atits elementary level of organization, is a response system -i.e.,a system which can hardly be described functionally withouttaking into account the input level.

Reflexes, synergies, feedbacks, and the like are basicfeatures of the organization of action. They represent intrinsicconstraints imposed by the motor system when a goal-directed action is to be put into execution. My point is thateach simple component of action should not be seen merely asan element of the large ensemble which subserves the goal,but also as a goal-directed action in itself. In other words,during the course of the execution of a goal-directed actionthe subject is permanently faced with subgoals to which hedirects subactions.

Arguments supporting this point can be drawn from theobservation of simple goal-directed actions, such as when aperson takes an object placed at a distance from his body.Though the resulting pattern of coordination is a single rapidmovement involving all the arm segments, the action oftaking an object can clearly be subdivided into at least twosubactions, reaching and grasping. Reaching is distance-covering action involving proximal joints, and it entails thecomputation of body-centered coordinates of the object'slocation in space. Grasping is a fine adjustment of the handand the fingers to the anticipated size, shape, orientation, and


Commentary / Ga\\iste\: Organization of action

use of the object, irrespective of its spatial location.This separation of a single action (taking) into two subac-

tions (reaching and grasping) becomes possible when theinput-output relationships involved in a given action areconsidered. If attention were focused exclusively at theoutput pattern generated by the motor system, the onlyproblem raised by the study of movement would be that offinding out the principles of coordination for the differentsegmental muscle commands. In fact, considering the input-output relationships introduces the need for another func-tional structure in the description of action. I have used theterminology of "visuomotor channel" (Jeannerod 1981) toexpress the idea that different aspects of the external world(e.g., in our case, different properties of the same object) areprocessed by specific neural systems and transformed intospecific motor commands. The visuomotor channels involvedin an action are assumed to be both mutually independentand mutually dependent. Their independence has to do withthe notion of parallel activation, whereby the input feedinginto one channel will be ignored by the others; their depen-dence pertains to a necessary law of synergy between thechannels to account for the coordination of the commandsresulting from parallel activation.

These points are illustrated by the following simple experi-ment. Subjects had to reach for and grasp real objects placed40 cm away on a table in front of them. Target objects werepresented through a mirror, in such a way that subjects couldsee only the virtual image of the object projecting at the tablelevel. The result was a situation in which the subject reachedfor the virtual image below the mirror without seeing hishand and met a second, real, object placed by the experi-menter at the expected location. This is usually referred to asthe "visual open-loop" condition (Held & Gottlieb 1958).

The particular feature of the experiment was that thetarget object could be suddenly modified in shape or inorientation without changing its absolute spatial location. Thisperturbation, which occurred randomly across trials, wasproduced by rotating the object at various angles with a smallmotor triggered by the onset of the reaching movement. Bythis technique, the same object (e.g., an ellipsoid object) couldappear either as an ellipsoid or as a sphere. Under otherconditions an elongated cylinder presented in the frontalplane could be suddenly rotated by 90° around its midpoint,thus assuming a sagittal orientation. Movements wererecorded at 50 frames per second on 16-mm cinefilm. Foreach movement, the duration and the velocity profile of thereaching component were measured. For the graspingcomponent the pattern of the anticipatory shaping of thefingers was also studied on the successive frames, by measur-ing the distance between the fingertips.

The film analysis revealed that the subjects had no problemin accurately grasping objects different from those for whichtheir movement was initially planned and directed. Further-more, the correct adaptation of the movement to the suddenchange appeared to be due to a very selective repatterning ofthe motor commands. The reaching component was notaffected as a function of whether or not the shape of thetarget object was changed at the onset of the movement. Theduration, maximum velocity, and shape of the velocity profileremained such that no significant difference could bedetected between reaching movements executed in normaland in "perturbed" trials. This was not the case, however, forthe grasping component. The anticipatory hand shaping wasmodified "in flight" when this was necessary for the newconfiguration of the object. There is apparently a completeredistribution of motor commands within the channel (orchannels) affected by the perturbation at the input level.Figure 1 shows movements directed either at a sphericaltarget object (A) or at a spherical object unexpectedly trans-formed into an ellipsoid object at the onset of the movement(B). On the left are represented the full-blown grasping

o o

Figure 1.

postures corresponding to the two respective trials. On theright is an indication of the time at which a change in handshaping can first be detected in a perturbed trial whencompared to a nonperturbed trial. Although 420 msec afterthe perturbation has occurred the grasping posture is stillsimilar for the two trials, a clear difference is visible some 120msec later (540 msec).

This experiment clearly shows that motor commands speci-fied by a certain visuomotor channel can be selectivelymodified during the execution of the movement. In addition,the fact that a change in object shape affects only thevisuomotor channel relevant for shape implies that thecompensation within the perturbed channel has. to beconstrained within the time limits required for execution inthe other, nonperturbed channels. The temporal frameimposed on all the channels participating in a given action (asdefined by the synergy rule for the movement) constrains theexpression of the control of individual channels by the ongo-ing (visual) input.

This is an example showing that the structure of motor actsdirected at an external goal is not only governed by motorrules. This structure is such that it allows a continuousmonitoring of the movement in terms of the goal itself. Thegoal shapes the parameters of the movement channel bychannel at the time when the program is built up beforeexecution and it eventually modifies these parameters duringthe course of execution. Input-output relationships thus deter-mine a further organizational principle superimposed uponthose described in Gallistel's book.

Dynamic servomechanisms are more fun:A critical look at chapters 6 and 7 ofThe organization of action

E. R. LewisDepartment of Electrical Engineering and Computer Sciences, University ofCalifornia, Berkeley, Calif. 94720

With its nose ringed with infrared sensors, the Sidewinderantiaircraft missile relentlessly homes on the hot exhaust portsof its target. Constantly keeping its steering vane at an angledirectly proportional to the imbalane in the inputs to itsinfrared sensors, it corrects for evasive maneuvers by thedoomed target until the inevitable final encounter. With thisvivid example, the reader is introduced to the servomecha-nistn, one of the three basic elements of action proposed inThe organization of action. As it is described here, theSidewinder missile belongs to a very elementary class ofservomechanism, often called proportional-error servo-



mechanisms. Considered deterministically, such servomecha-nisms can home perfectly on stationary targets under idealcircumstances; but it is well known that they cannot, inprinciple, home perfectly on moving targets (movement inthe case of the Sidewinder's target being its evasive maneuv-ers out of the path of the missile). Being stalked by aproportional-error Sidewinder, the wise pilot would knowthat the missile's corrections will lag slightly behind his ownevasive actions. Therefore, he might execute a giant loop,coming out of it flying as close as possible to the ground. Withany luck at all, the pursuing proportional-error Sidewinderwill be underground when it finally comes out of its loop.

Both the inertia of the Sidewinder and the viscosity of theair prevent the missile from turning instantaneously andtracking its moving target perfectly. Unless it can somehowanticipate the future positions of its target, it simply cannotmaintain zero tracking error when that target is takingevasive action. Probably the most obvious first step in anyattempt to anticipate the target's future positions is to esti-mate the angular velocity at which its position is divergingfrom the path of the missile. There are at least three clues tothat velocity immediately available to the control system ofthe Sidewinder. One is the rate of change of the error itself(i.e., the rate of change of imbalance of inputs to the infrareddetectors). Another is the rate of change of the signal drivingthe missile's steering vane; and the third is the rate of changeof the missile's actual course. If the bending of the steeringvane were in part proportional to the imbalance of inputs tothe sensors and in part proportional to one of these estimatesof the target's velocity of divergence from the missile's path,then the tracking error could be reduced or, under certaincircumstances, even brought to zero.

The point here is that with a relatively simple modification,we have made our hypothetical missile not only more effec-tive, but also more interesting. Unless a servomechanism isoperating in a quasi-static world, the dynamic factors asso-ciated with it (e.g., its own inertia and friction, the transientdynamics required of it, and the transient dynamics of theambient elements acting upon it) are quite critical. Theexisting theory of servomechanisms deals extensively withsuch factors; and, beginning with the pioneering work ofStark and his colleagues (1959), an extensive literature hasevolved dealing with these factors as they relate to neuromus-cular servomechanisms. However, in The organization ofaction, the reader is introduced neither to these factors nor tothe literature dealing with them. Instead, he is introduced tothe essentially static treatments of servomechanisms byFraenkel (1927) and by von Hoist and Mittelstaedt (1950).These treatments are elegant and definitely should be read byany student interested in neuromuscular servomechanisms; Iapplaud the author for including them in this book. However,they are very early endeavors and definitely do not bring thereader to the state of the art on the subject. After reading theadmirably clear presentations in chapters 6 and 7, the seriousstudent not already familiar with the study of biologicalservomechanisms should probe into the recent literature onthe subject. It will open his mind to the possibilities offascinating dynamic operations that might be carried out bythe neural networks of the central nervous system.

Behavioral plasticity, serial order, and themotor program

Donald G. MacKayDepartment of Psychology, University of California at Los Angeles, LosAngeles. Calif. 90024

As a psychologist concerned with the execution of skilled

behavior, including the highly complex and flexible coordina-tions underlying speech production, I welcome Gallistel'swell-written book on the organization of action. It bringstogether in one volume the classical problems of behavior andits causation, structure, and timing, and should prove espe-cially useful for graduate seminars. The one classical problemwhich is noticeably missing in The organization of action isthe problem of serial order: how do we generate preplannedsequences of behavior in proper serial order (when we do)and improper order (when we make errors). Besides neglect-ing Lashley's problem, Gallistel seems to have misread Lash-ley (1951) as providing a holisitc argument or solution to theproblem of serial order, which is undermined by more recentanalyses of, say, locomotion (p. 136). This neglect of Lashleyseems unfortunate, not just because of the importance of theserial-order problem but because Lashley in fact championedsome of the very mechanisms (even for locomotion) thatGallistel is championing now - e.g., systems of coupled oscil-lators, and priming (partial activation or potentiation).

Lashley's (1975) emphasis on the hierarchical organizationof motor mechanisms also echoes throughout Gallistel's book.However, Gallistel seems to forget about this hierarchicalstructure in his discussion of motor programs or schemas (p.368-71). Like many other investigators, Gallistel assumes thatthe engram for a skilled movement specifies the movementtrajectory in space, but not the neuromuscular activityrequired to achieve that movement in any one case. Thereason given for this "abstract program" assumption is behav-ioral plasticity in phenomena such as action constancy, wherea movement of the same form or function can be generatedby means of grossly different patterns of muscular activity; itis, for example, possible to sign one's name with either hand,either at a desk (with muscles of the forearm and fingers) oron a blackboard (with the muscles of the shoulder). Thecommon element generating the common form appearing inthe signatures is a set of coupled oscillators or Fourier compo-nents, which are independent of "which groups of musclesare to be active, in what order, and for how long," accordingto Gallistel (p. 370).

Recent experiments directly contradict this "abstractprogram" assumption: Klapp, Grein, Mendicino, & Koenig(1979) have shown that the motor-memory code for handmovements is both environmental and anatomic, as would beexpected in a truly hierarchic system, where high-levelcomponents specify spatial goals and lower-level componentsspecify muscle-movement goals. The fact that transfer fromone response mechanism to another is sometimes less thanperfect is also a problem for the "abstract program" assump-tion. Consider signing one's name with the unaccustomedhand, for example. One can transfer either the muscle-movement code, resulting in a mirror-image output (seeLashley 1951), or the spatial code, resulting in an approxi-mately normal signature. But in either case there is consider-able decrement in maximal speed and dexterity of form. So, ifan action sequence such as signing one's name is only repre-sented abstractly as, say, a set of Fourier components, inde-pendent of hand or other muscle systems, what preventsperfect transfer in writing with the unaccustomed hand? Andif muscle movements are not part of the long-term store, whyare we able to transfer the muscle-movement code at all so asto produce mirror writing with the unaccustomed hand?

The answer to the latter question is again that motorprograms are hierarchic in nature, with lower-level compo-nents representing specific muscle goals and higher-levelcomponents representing spatial goals. And the answer to thequestion of imperfect transfer is surely that the speed andvariability in the activation of motor components depends onthe degree of practice. For example, the components (nodes)at the muscle-movement level for forming letters with the



nonpreferred hand have not received the extensive practiceof those for the preferred hand, and therefore are activatedmore slowly and with greater variability. By way of contrast,perfect bilateral transfer of practice occurs when the lower-level nodes have already received asymptotic levels of prac-tice. An extreme example is skill at chess, which transfersreadily to the accustomed hand, since the muscle-movementnodes for moving chess pieces or any other small objects havereceived extensive practice since early childhood. A higher-level example involving the same principle is skill in produc-ing a sentence at maximal rate, which transfers withoutdecrement to producing a translation of the sentence in theother language of a fluent bilingual (see MacKay & Bowman1969). Here the common elements represent high-levelconcepts, while the divergent lower-level nodes with asymp-totic degrees of practice represent the words and their pho-nology as well as the muscle movements for realizing thespeech sounds of the words.

Of course, Gallistel does make reference to hierarchicalorganization in discussing other aspects of behavioral plastici-ty, such as stumble-preventing reflexes in the cat, context-dependent phototaxes of the coastal snail, and response gener-alization in humans. Here his account, as far as it goes, seemsfundamentally correct: higher-level nodes representingconcepts such as "escape shock" and "withdraw the righthand" (in Wickens's 1938 study of response generalization)must simultaneously prime several (in this case antagonistic)nodes at the muscle-movement level. These motor nodes alsoreceive varying degrees of priming from other sources, andwhatever node receives the greatest degree of primingbecomes activated, triggering the corresponding musclemovement. As Gallistel points out, these "other sources" mustcompute that relation between body space and neuromuscu-lar space, thereby ensuring that a signal commanding upwardmotion of the fingertip produces extensor excitation when thehand is oriented palm down and flexor excitation when it isoriented palm up (p. 393).

What is notably absent in this account is the triggeringmechanism for selecting and activating the node with thegreatest degree of priming in the domain of primed motornodes. And as Lashley (1951) pointed out, the triggeringmechanism in the case of complex behaviors must have accessto the syntax of the preplanned action, so that its componentsare activated in proper serial order. However, we must surelyforegive Gallistel on this point, since neither Lashley noranyone else has conclusively worked out the triggering mech-anism for complex behaviors and since a well-written book onthe remaining problems in the organization of action is surelyaccomplishment enough.

Where's the action?N. J. MackintoshLaboratory of Experimental Psychology, University ot Sussex, Brighton,BN1 9QG, England

Gallistel has brought together an important group of papersand has written a fine book about them. He is right to claimthat classical physiology and neuroethology have developed anumber of principles underlying the organization of patternsof movement, and these principles undoubtedly help toresolve some of the difficulties involved in developing acomprehensive theory of action - but not, I suspect, all. I shallconfine my remarks to a single issue. The book deals, we aretold on the jacket, with "the principles by which complex,purposive, and intelligent behavior is generated." To astudent of animal learning or conditioning this can imply but

one thing: that we will be given a theory of instrumental oroperant behaviour. There is no question that we need one. AsGallistel says in the book: "When a representation of someaspect of the world has been laid down in memory, it mayhelp to guide and control the animal's subsequent actions.The question is . . . How can knowledge control action?" (p.335). It is a question that has haunted cognitive theorists eversince Guthrie charged Tolman with leaving his rats buried inthought. But Gallistel does not solve more than a small part ofit (and that the easiest), for the solution he proposes is toexplain instrumental action in terms of classical conditioning.

In classical conditioning, animals learn about the relation-ship between a stimulus and a reinforcer, and this stimulus,by virtue of its association with the reinforcer, comes to elicitresponses related to those elicited by the reinforcer itself.Although these responses were long thought to be confined tosimple reflexes or autonomic reactions (such as blinking orsalivating), the discovery of autoshaping (Brown & Jenkins1968) made it clear that the movements of an animal throughspace could also be classically conditioned. An appetitivereinforcer may elicit approach, and an aversive reinforcerwithdrawal, and both these reactions can be classically condi-tioned to stimuli associated with those reinforcers. Classicalconditioning of approach and withdrawal may then appear tomimic true operant behaviour: that is to say, much of thebehaviour observed in ostensibly operant experiments may infact be classical in origin. When a rat is required to traverse amaze in order to obtain food in the goal box, the experimentermay believe that he has arranged an instrumental contin-gency between the rat's behaviour and the delivery of thereinforcer, but the contingency actually controlling the rat'sbehaviour may be the classical one between the stimuli of thegoal box and the reinforcer. Deutsch's (1960) theory of mazelearning, which Gallistel advances as a theory of instrumentalaction, proposes just this: various stimuli in the maze areassociated with food, and each of these stimuli in turn comesto elicit an approach response. It is ingenious, plausible, andreadily instantiated in mechanical terms, but it is a theory ofhow stimulus-reinforcer contingencies affect animals' behav-iour; it does not explain how animals learn about the conse-quences of their actions and modify those actions according-

ly-The question is whether we need such a theory. Perhaps we

could explain all cases of apparently instrumental learning inthe sorts of terms proposed by Deutsch. Perhaps there is nosuch thing as true operant behaviour. Certainly, there havebeen theorists who have advanced this argument (e.g., Bindra1978, in this journal). But Deutsch himself never did, and hewas surely right. There are numerous examples of instrumen-tal conditioning that cannot easily be reduced to the classicalconditioning of approach to or withdrawal from stimuliassociated with appetitive or aversive reinforcers. Both Miller& Konorski (1928) and Grindley (1932) saw clearly the sort oftask that was required to establish that instrumental condi-tioning was a process distinct from classical conditioning, andboth studies showed that a restrained dog or guinea pig couldlearn to perform an arbitrary, discrete response, such aslifting a leg or turning the head, in order to obtain food.There are other, more modern examples (cf. Mackintosh &Dickinson, 1979). A plausible account of such cases of genuineinstrumental conditioning, and one of which, from briefhints, one suspects Gallistel would approve, is that animalscan learn that their actions are associated with certain conse-quences, just as, in the case of classical conditioning, theylearn that external stimuli are associated with particularconsequences. But the problem then becomes one of explain-ing how this knowledge affects action. How does a represen-tation of the relationship between an action and its conse-quences determine the performance of that action?



A small fly in some beneficial ointment

P. M. MilnerDepartment of Psychology. McGill University, Montreal. P.O.. Canada H3A1B1

Gallistel has provided an excellent synthesis of all the pointsthat I consider most important for understanding behavior. Icould document my concurrence with his conclusions byreferring to several of my papers. For example, in 1959 I gavea talk that described just such a hierarchical model as Gallistelpresents, with preorganized action systems for walking,grasping, chewing, and so forth, and illustrated it with adiagram of a six-tier response mechanism with a drive at thetop level and motor units at the bottom (Milner, 1961; Fig. 4,p. 120). Each level facilitated (i.e., potentiated) several alter-native action units at the next lower level, one of which wasthen selected and fired by sensory input available at thatlevel, and so on down to the motor units where the sensoryinput was mainly from muscle spindles (less controversialthen than they are today).

The talk was published in a book somewhat ironicallycalled Current trends in psychological theory. Obviously thetrend was not as current twenty years ago as I imagined.Perhaps it was to avoid having his book dismissed as toospeculative that Gallistel chose to include the long (andsometimes long-winded) classical articles. His own style isclear and lively, and the book would have been more readableif he had written it all himself. In fact, the only fly of anysignificance that I found in the ointment was introduced bytwo of his eminent coauthors, von Hoist and Mittelstaedt(1950).

Von Hoist is puzzled that flies are not paralyzed by theoptokinetic reflex and postulates that the reflex is cancelledby a copy of the motor command for self-produced move-ments. But the optokinetic reflex is relatively slow; a fly canalmost certainly move too fast for the reflex to follow.Moreover, if the visual world moves suddenly, flies do not sitaround readjusting their posture; they depart from the scenewith as much brio as they can muster. The question von Hoistshould have asked is why flies do not scare themselves into fitsevery time they move.

No self-respecting ethologist would pay any heed to what afly did in the optokinetic-reflex apparatus. In real life themovement of a visual image depends on the orientation anddistance of the objects in the field, as well as on the velocity offlight. How can a simple efference copy compensate for suchmultiply determined and variable input?

Finally, the experiment cited to dispose of the alternativetheory that the reflex is depotentiated during movement isquite inconclusive. The fly with inverted head is gyratingunder the influence of the optokinetic reflex (malfunctioningthough it may be); it is not making "spontaneous" move-ments. Neither theory predicts interference with reflexesgenerated by outside movement, so the fly's predicamentdoes not help us to decide between them.

At the human level it is false to assume that only theefference copy allows us to decide whether a movement isobjective or self-produced. Most regular railway travellershave experienced the illusion produced by the departure of atrain on the adjacent line. The feeling of movement as onelooks out of the window is quite compelling and there is analmost physical shock as the last carriage passes and thestationary scene behind is revealed, bringing us to a suddenhalt. We succumb to this illusion in spite of the lack ofefference or any nonvisual sensory indication (vestibular,pressure from the seat, etc.) that we are moving. We knowalso that the train outside is not a fixture, yet we are so used tointerpreting movement outside the window as movement of

the train that we discount all these cues.An equally compelling illusion is created by 360° movies

taken from a moving vehicle. Our experience tells us thattrees and houses do not stream past; it must be ourselves whomove. Clearly, at the human level, past experience is moreimportant than any efference copy in determining how weinterpret visual input.

We are always aware of the true orientation of visualobjects in relation to our body. The lack of perceived motiondoes not fool us into thinking that what was straight aheadbefore an eye movement is still straight ahead afterwards(though it is not obvious that von Hoist realised this). It seemsthat there must be a side branch of the visual system devotedto the detection of movement and the efference copy musttranslate the whole visual image in that branch to the positionit is expected to assume after the movement. If it does notappear in that position there is a perception of movement andan alarm is raised to draw attention to the phenomenon.Translation of the visual field requires a more complicatedcomputational network than simple subtraction of motorcommands. My guess is that it involves the superior colliculus,the pons, and probably the cerebellum, which is richlysupplied with positional information, both efferent and reaf-ferent.

The efference-copy idea is an important one, I am sorrythat Gallistel chose to present von Hoist's very confusingtreatment of it.

Finally, I would like to comment briefly on Gallistel'sspeculations on how cognitive maps are read. It is a problemthat I have spent many years contemplating.

Useful as the idea of the cognitive map has proved to be, Isuspect that Tolman may have done psychological theory adisservice when he coined the expression. It is too tempting totake the metaphor literally and imagine something like a roadmap spread out on the hippocampus, or wherever. Fromthere it is a short step to imagining a map reader who knowswhere he wants to go and consults the map to find out what todo.

In geographical maps response instructions are implicit, orcoded, but there is no reason that the brain should use thesame code. It probably contains much more explicit informa-tion. In fact, I believe the "map" consists of a large number ofstatements or response associations of the form "Go 2 kmalong this route and you will come to Howard Johnson's" or"Bark twice and the door will open." A better name for thismight be a gazetteer of expectancies.

I do not believe this map or gazetteer is consulted todiscover the response; rather, it is the other way round. Everysituation presents a choice of responses, and the gazetteer isconsulted to discover the consequences of each. Because theanimal already has a plan for a response, the question of howto translate from a map to a response does not arise. If theassociations with the planned (or potentiated) response arefound to be of no value for reaching the goal, that plan is notexecuted, and the gazetteer is once more consulted to discoverwhere another of the possible responses will lead. When aresponse is found whose outcome has associations with thegoal, the potentiated response is given the green light andactivated. If any of the possible responses have no associa-tions, the animal may explore so that some are acquired, andthese associations are then entered into the gazetteer forfuture reference.

Of course, animals cannot go through this vicarious trial-and-error rigmarole every time they make a response. Infamiliar situations the response first thought of is the one mostoften made before, so it is tested first and may even bereleased automatically, without any consultation. If thatsounds like our old bete noire, stimulus-response association,that is just what it is. The fact that it is no good for explaining



latent learning or problem solving does not mean that S-Rlearning never occurs under any circumstances. It is as good amodel as any for explaining automatic behavior.

Deutsch's (1960) theory of problem solving, which is theone presented by Gallistel, has several limitations, the mostserious being that it sidesteps the general question of responsetranslation by assuming a single, all-purpose approachresponse, elicited when a stimulus whose map referencereceives drive activity appears. If something other thanapproach is required (tail wagging, for example), there is noway of representing that on the map, and no way of reading itoff the map. Deutsch's model is useful for illustrating thedifficulties that must be tackled and the general principles tobe considered in a solution, but it is not easy to see how theconcepts translate into physiological mechanisms.

It is probably clear from my commentary that I do notthink Gallistel has quite written the perfect book on thesubject of action systems, but it is close. The main ideas are allthere, and I am delighted to see them set forth so articulately.I hope the publication will ensure that this way of thinkingabout psychological problems will be more widely acceptedin the future.

Hierarchical structures in the organization ofmotor behaviorsLewis M. NashnerNeurological Sciences Institute. Good Samaritan Hospital & MedicalCenter. Portland, Ore. 97209

The conceptual emphasis of Gallistel's book elicits mycommentary, not so much upon the myriad of important butspecialized details as upon the ability of the book to accom-plish one of the expressed purposes of the author: "toconvince psychologists and behavioral neurobiologists that theconceptual gap between muscles and motivation is not theyawning chasm most of us imagine." Gallistel has assumedthe role of advocate rather than reviewer or critic. He hascarefully chosen a series of historically important papersbased upon motor-system research and has interwoven thesewith his own thoughts to advance the concept of a "latticehierarchy." At a time when our information concerninganatomical components seems to outpace our ability tocomprehend the workings of the system, in-depth presenta-tion of a physiologically relevant organization concept isextremely useful. Because this book represents the effort ofone mind rather than a collection of more loosely connectedchapters by separate individuals, its cohesiveness more thancompensates for a lack of representation of alternative view-points. For example, Gallistel quietly but in no uncertainterms dismisses the reductionist approach to the understand-ing of CNS organization.

The reader will find a natural subdivision of the book intotwo parts, although this separation is not reflected in itsformal organization. In the opinion of this reviewer, the firstsubdivision is most successful in accomplishing the statedobjectives of the author; it carefully builds upon very basicprinciples of motor organization in order to demonstrate theconceptual power of hierarchical principles. The secondsubdivision is smaller in scope and less exacting in its attemptto generalize concepts derived from motor organization toencompass cognitive levels of action such as motivation andlearning. While this section will probably not convince thereader to the same extent as the previous one, it is useful inproviding a stimulus for further thought.

The first subdivision of the book is a sequence of carefullyorchestrated articles by such well-known psychologists as

Sherrington and von Hoist. Through the course of ninechapters, a series of experimental observations and mechani-cal analogies is used to show how three very basic organiza-tional structures, the reflex, the oscillator, and the servomech-anism, interact to generate behaviors more complex thanproduced by each separately. Perhaps the finest achievementof the book is in building these ideas into several principles ofhigher-level interaction, principles which are often alluded toelsewhere in the literature but with less than full understand-ing. Specifically, Gallistel describes how "competitive" inter-actions among structural units operating at the same hierar-chical level, from whence arise the "lattices" characteristic ofthe hierarchy, yields a much wider range of possible behav-iors. Furthermore, he demonstrates how selective higher-levelpotentiation of lower-level behaviors, as compared to directcommand of these behaviors, enables a system that is fixedstructurally nevertheless to exhibit highly flexible andperhaps "intelligent" behaviors when it operates within achanging environment.

In summary, The organization of action: A new synthesiswill be an excellent conceptual source book for the studentinterested in organized actions of the central nervous system.It should also prove of value to the researcher who, over theyears, has had piecemeal exposure to concepts of organiza-tion, but has not had the opportunity to "solidify" theseconcepts within his own mind.

A basis for actionAllen NewellComputer Science Department, Carnegie-Mellon University, Pittsburgh, Pa.15213

Gallistel puts forth his book as providing the basis on whichwe scientists should organize our future actions. It is crafted tocapture our attention, communicating by its form as well asby its content, and containing enough contrasts to confound asimple reading. I found the result pleasing, by and large.

The book strongly invites attention to its overall message,rather than to its scientific details. On its own account, bymany caveats, though the scientific content is to be takenseriously, it is fundamentally in the service of the overallmessage.

I read the message as follows: (1) The central ingredientsexist for constructing a theory of the organized actions ofanimals, including man. (2) These ingreidents form a basis, inthe sense that from them can be composed all the actions ofthe animal. (3) These ingredients have been available in thescientific literature for a long time. (4) Yet this synthesis isnew, because we cognitive scientists have failed to recognizethat these ideas exist.

I found pleasing the use of original articles to convey themain substantive thrust of these ingredients. It is good to bereminded, with the pungency of the originals, of relevantwork one already knew (for me, Sherrington on reflexes andWeiss on salamander transplants). It is doubly good to beintroduced to neat work from the past that had somehowslipped by (von Hoist on fish fins) or that had lain beyondone's earlier scientific horizon (Wilson on insect gaits). It iseven good to have one's position challenged on work longsince studied and set aside (the Deutsch model), even if oldopinions more or less prevail.

The substantive proposition of the book can be capturedalmost entirely by enumerating the proposed basis. Itselements are the reflex, the oscillator, and the servo. Its mainorganizing principle is the control hierarchy. Its controlprimitive is potentiation and depotentiation. There is also a



principle of the clever simple solution (illustrated moststrongly by insect locomotion): simple mechanisms can solveamazingly complex behavioral problems for the organism.This principle bolsters the view that a simple (bio)mechanoset suffices for obtaining intelligent action in the face of avariable environment.

At this point I do not know quite what to say. I'm afraid Iam about to carp. Since I feel almost entirely positive aboutthe book and its potential effects, this is definitely not a goodthing.

Nevertheless, here is the carp - and then I'll try to riseabove it. Gallistel does not practice what he preaches. At thelevel of the message, everything that he says is familiar incognitive psychology. Not only that, but it has been clear fortwenty years. There is no problem with the homunculus; withthe composition of action out of a procedural basis; withwhether mechanisms can yield intelligent and purposiveaction; with autonomous signal generators, hierarchy,multiply evoked subsystems, gated control, generalizedcontrol systems, mechanically realizable representations; andso on. For all of this, there is no problem at the level at whichhe treats the issues. For someone who casts his book to chidethe field for not heeding existing science - as in his contra-puntal treatment of old writings and declared new synthesis -he has not himself attended closely to what is known andunderstood in the field he seeks to instruct.

I have stressed the level of the message. At levels ofspecificity, detail, and task scope beyond those in the book,there are important issues on all the above topics. Thedifficulty is not a failure to be concrete; the book succeedsthere admirably. The difficulty is that it is illustrative. In fact,the trouble is that the book is a handwave - well executed andbased on real data, but a handwave nonetheless. It is reminis-cent of Hebb's Organization of behavior (1949), a workremarkably similar in motive, style, and even argument -trying to get psychologists to take the neural level seriously.(It is not cited, interestingly enough.) Hebb's was one of thegreat handwaves in psychological history, and its impact wasimmense and deserved. At that historical moment, Hebb'soverall message was a breath of fresh air. The new orientationcounted; the details didn't.

In a kiloword review I cannot document my claim that thecognitive world already understands the macro lessons thatGallistel seeks to tell us. Also, I am not my brother cognitivepsychologist's keeper. I will not aver that all psychologistsknow what they should about modern artificial intelligence,robotics, computer science, and control engineering, toinform their more direct knowledge of cognitive models anddata. But there are plenty that do.

What would I have liked? Perhaps a detailed critique ofthe biological plausibility of Saltzman's (1979) attempt atsynthesis of sensorimotor representations (though that mayhave emerged too late). Perhaps a discussion of the nature ofpotentiation as one type of control primitive against what weknow of the total needs for control, say, from programminglanguages. Perhaps a discussion of the biological plausibilityof various bases for composing functions, out of the indefinitevariety of ways that are known for this besides Fourierdecomposition (e.g., all the orthonomal polynomials, manyother transforms, etc.). Perhaps even my old favorite (Newell1980) of how the type of action system under discussioninterfaces or melds into a symbolic system. Mostly, I think, weare ready for actual theory that can be seriously taken to taskand then improved. We do not need to be convinced at thelevel at which Gallistel seeks to convince us.

But enough. The motor system certainly has a distributedcontinuous control. It is due for much more attention in thecoming decade. And much will be learned thereby that willaffect and enrich our view of the total cognitive system.Gallistel makes the case that the time is ripe (to squeeze an old

cliche). And his work will certainly help bring on this nextwave of research.

Behavioral flexibility and the organization ofactionDavid S. OltonDepartment of Psychology, The Johns Hopkins University, Baltimore, Md.21218

Gallistel's "new synthesis" is a welcome addition to thecurrently available descriptions of animal behavior. Althoughmany of the earlier models can be adapated in some post hocway to account for the types of behavior discussed by Gallis-tel, these models still have difficulties because they werenever designed to predict the flexible, organized aspects ofbehavior which are the focus of the work here. As examples ofthese intelligent behaviors become more and more frequent,both from the laboratory and from the animals' naturalhabitats (see, for example, Kamil & Sargent 1981), we desire adescription of behavior that focuses directly on them, ratherthan including them as an afterthought.

I was particularly interested in the discussion in chapter 11.The idea that knowledge (nodes and connections) in a cogni-tive map can exist without specifying any action (direction ofmovement) is an excellent one, particularly in the context ofthe more cognitive emphasis that currently characterizespsychology. The question, of course, is how we get from theseunobservable cognitive processes to observable behavior.Gallistel says: "If we know both what an organism wants andwhat it knows, then we feel intuitively that we can predictwhat the organism will do" (p. 351). But how well do theseintuitive feelings actually lead us to the correct predictions?In some cases, documented in chapter 11, appropriate knowl-edge plus motivation does produce intelligent action, such astaking shortcuts to the desired goal (see also Becker & Olton,in press; Becker, Olton, Anderson & Breitinger, in press). Butsuch is not always the case, and the literature is replete withexamples of animals exhibiting very inflexible and unintelli-gent types of behavior.

Some of these examples may be found after specific train-ing, as in Maier's "frustration" experiments with the Lashleyjumping stand (Maier 1949). For some rats, the first discrimi-nation was solvable (i.e., one stimulus was always correct).These rats rapidly learned to jump only to the correctstimulus. For other rats, the first discrimination was notsolvable (i.e., each stimulus was sometimes correct and some-times incorrect, and the rat was unable to predict whichwould be the case for any given trial). When subsequentlygiven the discrimination that could be solved, these ratspersisted in choosing incorrectly, in spite of indications (suchas changes in latency and posture when making choices) thatthey had learned which stimulus was correct and which wasincorrect.

Inappropriate choice behavior has been documented in avariety of other situations as well (see Olton 1979, pp. 584-85,for examples). Most importantly, these experiments did notinclude any specific training experience (like that of Maier's[1949] experiments) prior to the discrimination task. Nonethe-less, the animals were notably inflexible, running into walls oroff mazes, much as the more stereotyped, mechanical modelsof animal behavior might have predicted.

Finally, a particular animal can be trained to exhibitconsistently either a relatively flexible or a relatively rigidbehavior in a variety of different experimental situations. Theideas of learning set, transfer of training, functional fixedness,learned helplessness, learned success, etc. all imply a generalpropensity toward either insightful, adaptive, and intelligent


Commentary/GaMisteh Organization of action

new approaches to a problem or a rigid, maladaptive, andinappropriate perservation of old habits.

Thus I ask the following question: when knowledge andmotivation combine to produce action, what are the variablesdetermining how adaptive and flexible this action will be?Something other than the components of the present theoryseems to be required, something that reflects the "creativity"with which an animal approaches a given situation. Howwould Callistel incorporate such a variable into his organiza-tion of action? How is it established, and does it affect thedirection of action when behavior ensues?

Giving behavior to psychologyRobert R. ProvineDepartment of Psychology, University of Maryland Baltimore County,Calonsville, Md. 21228

In response to the behaviorist revolution, it has been said that"psychology, having first bargained away its soul and thengone out of its mind, seems now . . . to have lost all conscious-ness" (Burt 1962, p. 229). Amid the turmoil about psycholo-gy's state of mind, it went unnoticed that there was little"behavior" in behaviorism or elsewhere in psychology. Withfew exceptions (e.g., linguistics and species-typical behavior),contemporary psychology is devoid of fine-grain analyses ofmotor behavior. Where is our choreography or grammar ofmovement? Where is our "abnormal psychology" of move-ment disorders? The motor chapter of the typical textbook ofphysiological psychology has little to offer but a tired descrip-tion of the alpha and gamma motor systems and simple andcomplex reflexes. These cursory treatments, apparentlyadded only for "completeness," bear no relevance to the restof the book. They do not even mention the contemporaryresearch on endogenous pattern generators that has revolu-tionized thinking about motor control. Man and beast areinstead treated merely as reflex machines. The empiricalphilosophy which gave rise to modern Western psychologyproduced a vigorous psychophysics and psychology ofperception, learning, and cognition. Sadly, on the motor side,the empirical tradition generated only that meager parcel ofmotor behavior, the response. The relative neglect of motorprocesses also stems from the fact that the development ofmovement and its neuromuscular "machinery" is relativelyindependent of experience, (Provine 1979, in press) and thatonce movement disorders are produced the prognosis forrecovery is often poor. Motor behavior has not earned asignificant place in a psychology devoted to cataloguingenvironmental influences on behavior.

Motor processes deserve a more prominent position in thebehavioral sciences. Indeed, the senses and the nervoussystem evolved in the service of movement; without move-ment, they would confer no selection advantage. There are nointelligent turnips. Neuroembryological analyses also indicatea unique and important position for the motor system (Pro-vine 1976). The precocity of motor processes is unrecognizedby most developmental psychologists, although it was firstnoted by Preyer (1885) almost a century ago. Embryos oftenact before they react ("spond" before they respond), andspontaneous (nonevoked) processes are probably responsiblefor most embryonic motility. Furthermore, the efferents ofsome central neuronal circuits develop before they receivetheir afferents (Bruce & Tatton 1980; Stein, Clamann, &Goldberg 1980). The sensory and supraspinal systems may not"capture" and modulate the freewheeling motor systemsuntil the basic structure of the nervous system is well blockedout. These behavioral, physiological, and anatomical findingsforce a reconsideration of developmental accounts that

depend upon environmental "instruction" as a significantdeterminant in the genesis of neuronal circuitry. At a moremolar level, movement is also important in determining theenvironment and experience of a given organism. Piagetrealized this and continually stressed the interdependence ofmotor and cognitive development. This interplay was centralto his view of the child as experimenter, not passive meta-physician.

Gallistel's book should help bring motor processes andrelated topics to the attention of psychologists and makerelevant areas of psychology intelligible to neurophysiologists.The book makes contributions at several levels. It providesthoughtfully selected papers and excerpts from the history ofmotor control (e.g., Sherrington, von Hoist, Weiss, Wilson,Fraenkel), some of which are relatively unknown or difficultto obtain. Gallistel's perceptive introductions and analysesmake the reprinted material especially useful. He successfullytranslates early ideas and terms into the parlance of contem-porary neuroscience. An excellent glossary of frequently usedbut often undefined terms is even included. A second contri-bution is the idea that behavioral control is exercised throughthe selective potentiation of functionally coherent subsets oflower units of action. This approach provides a commonground for psychologists and those with more molecularinterests in behavioral neuroscience. Other topics covered arecentral to motivational theory, perception, cognitive psychol-ogy, development, and ethology. I highly recommend Gallis-tel's book as a unique and useful historical introduction,source book, and synthesis of a wide range of topics concern-ing "the organization of action." It deserves a wide audience.

Can mental representations causebehavior?Edward S. ReedCenter for Research in Human Learning, University of Minnesota, Minneapo-lis, Minn. 55455

Gallistel's book is an extremely important contribution to thetheory of action. He has succeeded admirably in synthesizingseveral centuries' worth of knowledge into a clear presenta-tion. Although my comments below will be highly critical,they should not be seen as detracting from the great value ofGallistel's work. Without Gallistel's lucid and comprehensivereview, the important issues I attempt to discuss below couldnever have been raised.

Gallistel's work is an impressive synthesis, but it is by nomeans "new," as he claims; he is misled by the widespreadmythology of the "novelty" of psychobiological ideas whichare at least three centuries old (Reed 1980). This misappre-hension obscures deep problems in Gallistel's theory. Gallistelhas set out to answer, in as scientifically materialist a way aspossible (p. 4 ff.), the question Descartes first raised in hisPassions of the soul (1649): how do ideas (mental representa-tions) cause behavior? Like Descartes, Gallistel proposes atwo-system answer: the cognitive system selectively poten-tiates the machinery of the body. We are told (p. 358) that,although no one has ever had the faintest idea how ideascould cause actions, this is of no great concern to the theory.Personally, I think three centuries of inability to answer ascientific question demonstrate that the question itself issuspect. Certainly, Gallistel should address this perennialfailure in a more serious manner than his vague and desultoryexposition on pages 388-90. But even granting that Gallistelmay yet solve the problem that defeated Descartes, Kant,Miiller, Sherrington, and others, there are further problemswith this old synthesis in new guise.



The most frequent reason given for hypothesizing thatmental representations cause behavior is an argument fromexclusion (see Darwin 1958, p. 84). For example, Gallistelclaims that because no other explanations of Maier's (1929)experiments are viable, cognitive maps must be hypothesizedto explain rat detour behavior (p. 338). Crudely put, thegeneralized form of this argument is: mental representationsare hypothesized to account for whatever knowledge ispossessed by animals that is not explicable by appeals to habitand experience. Representations are nowadays invariablysupposed to explain novel and insightful behavior, instancesof action in which animals in no way repeat earlier episodesof behavior. Like the predictions of a scientific theory,representations are conditionals ("If I do X, then Y willoccur") and can support counterfactuals (X need not be thecase; Fodor 1975). These aspects of representations thusprovide an appearance of explanatory power. For instance,the hypothesis that an animal possesses a cognitive mapseemingly accounts for all the spatial knowledge that animalhas, especially its knowledge of the areas of the environmentnot now being experienced ("If I move in that direction, thenI will experience something like X").

There are at least two serious difficulties with this sort ofexclusion argument for representations. First, it makes cogni-tive psychology parasitic on behaviorism. Ever sinceChomsky (1959), cognitivists have been hypothesizing mentalrepresentations whenever their favorite (or most reviled)behaviorist's theory fails. Chomsky's arguments againstbehaviorism are largely correct, but Chomskyan accounts oflanguage learning have been seriously weakened by thisabsurd strategy of standing Skinner on his head. If behavior-ism is wrong, then behaviorist accounts of experience arewrong and nothing can be inferred from failures to explainusing those accounts. Hypothesizing entities, such as mentalrepresentations, is a perfectly legitimate research strategy,but one's hypotheses should be designed to generate tests andto explain facts, not to explain away previous ignorance. [Seealso Chomsky: "Rules and Representations" BBS 3(1) 1980.]

The second problem with basing arguments for mentalrepresentations on the poverty of experience is much moreserious than the first one. By its very structure, the argumentfrom exclusion makes the origin of representations (in on-togeny or phylogeny) supernatural. It is not possible formental representations with the strength of counterfactualconditionals to have evolved, as a simple example, drawnfrom Lee (1980), will show. Cannets are seabirds who prey onfish by diving to catch fish swimming near the water'ssurface. In diving, what gannets usually do is drop, allowinggravity to accelerate their bodies while they use their wings tosteer. In order to avoid deadly damage to their bodies, thesebirds must retract their wings before the wing-trunk junctionhits water. However, if they retract their wings even a briefmoment too soon prior to entering the water, they will misstheir prey. In short, for gannets, there is an extremely brief"window" of success in fishing. How can this single, butprecise, behavior of wing retraction be explained?

Gallistel apparently would explain gannets' wing-retrac-tion ability by hypothesizing that these birds have a spatial ortemporal representation of their diving trajectory, a represen-tation which selectively potentiates reflex mechanisms ofwing closure. For each dive the birds have to compute arepresentation with the following content (but not form): "If Icontinue to fall at the present rate I will hit the water at timet, so I must retract my wings at t-A." How could these birdshave evolved the ability to represent this counterfactual?Birds who actually experienced hitting the water would havedied before they could live to tell their tales. This selectivemortality can explain why gannets rarely smash themselves todeath, but it cannot explain how they could use representa-tions predicting that danger to control their actions.

Although the hypothesis that animals form mental repre-sentations or "models" of the world (Pantin 1965) is widelyadhered to, no one has ever explained how those "models"could convey information about nonactual states of affairs("If I don't hide, that tiger will eat me, so I hide."). Yet,according to Gallistel, representations are to be hypothesizedprecisely in order to explain how animals come to knownot-yet-actual or not-yet-experienced states of affairs. To besure, some representations simply store past experiences(memory), but the explanatory power of representationalhypotheses comes from the alleged ability of representationsto go beyond the information given, and therefore to explainnovel behavior in animals. For example, Gallistel (p. 358) andothers wonder whether the rat's representation of space is"Euclidean." What rat (or person) has ever experienced twoparallel lines extended to infinity and then checked to see thatthey nowhere intersect? How might a rat (or a person) haveinvented such a hypothesis in the first place? Cognitivists, likeGallistel, agree with behaviorists that hypotheses must comefrom experience or from heredity. Ex hypothesi, representa-tions with the complexity of geometry do not come fromexperience; hence, they are (at least in part) innate. But thisjust makes matters worse: for natural selection to haveproduced rats who hold to Euclidean geometry there musthave been, at some time, a population of rats whose represen-tations of space varied, so that selection could operate andpick out the most successful representation. So Gallistel mustnow explain the origin of rats whose representation of space isEuclidean, Lobachevskian, Riemannian, and so on!

I take it that the above is a reductio ad absurdum, not ofmental-representation hypotheses as such, but of the argu-ment that representations (or animals) go beyond the infor-mation given. Animals act as if they were considering coun-terfactuals ("If I do X, then Y; not X, then Z; Y is preferable toZ, so I will X"), but this does not entail that animals go beyondtheir experience, or that they have mental representations.Rather, it implies that perceptual information is far richerthan behaviorists or cognitivists have allowed, and thatperception itself supports these counterfactual seemingepisodes.

Gannets, to return to Lee's (1980) account, control theirwing retractions by initiating movement according to amargin value of a dimensionless optical invariant r'(t) speci-fying whether their dive will be successful. Any system whosebehavior is a function of r(t) or r'(t) (I call it the "Leenumber") acts as if it were predicting a future possible stateof affairs. Whether or not gannets represent Lee numbers tothemselves is anybody's guess, and irrelevant here, because,representation or not, the explanation is due to the Leenumber. What is relevant is that, by changing their behaviorwhen -r(t) reaches a marginal value, the birds change theiractual flight course, so that the previous Lee number speci-fied a potential, not an actual, collision. (For a more detaileddiscussion, see Turvey, Shaw, Reed, & Mace, in press.) Notealso that Lee numbers are an environmental resource (beingfacts of optical flow) to which animals might become adaptedby natural selection. The comparative zoology of eyes in factsuggests the existence of strong selection pressures for thedevelopment of visual systems capable of detecting opticalflow (see Land 1980; Salvine-Plawen & Mayr 1977).

From the biological and materialist point of view espousedhere, and apparently favored by Gallistel, the strategy ofhypothesizing representations that go beyond the informationgiven is pernicious: it can only explain why animals live infantasy worlds, not the real, evolving world. If Gallistel eversolves Descartes's question about how representations guideactions, the representations involved will be accuratelyencoded models of the real environment, and the informationwithin them that enables animals to anticipate the conse-quences of their behavior.



Behavior ignoredPeter C. Reynolds1660 North LmSalla Slroel, Chicago, III. 60614

Although Gallistel's book is less a synthesis than a compen-dium, it does cover old ground in a competent and clearlyexplicated way: hierarchy and heterarchy, reflex and servo-mechanism, coupled .oscillators, and Fourier transformationsare all here, as are those oft-reprinted authors, Weiss, vonHoist, and Sherrington, Yet, far from going beyond thesetraditional concepts, Gallistel stays firmly within the rational-ist, individualist, and ahistorical framework of Americanexperimental psychology. Gallistel's animals have no socialbehavior, and they live in an ecological vacuum. They havemotivation but no emotion. They have motor skill but nocommunication. Ethological authors are cited to bolster thecritique of naive behaviorism and reflexology, but the mainimport of the ethological approach - that behavior has asocial context and a natural history - is nowhere to be found.The environment intrudes in the case of the digger wasp, butonly to illustrate the abstract concept of mental maps; andhippocampal function - the only excursion into limbic fore-brain mechanisms - is reduced to the point-by-point repre-sentation of Euclidean space. There is not even a hint thatsocial action cannot be reduced to the potentiation of motoracts within the single brain, much less awareness that socialaction has organizational principles of its own. Moreover,Gallistel's view of cognition is unclouded by a single ethologi-cal doubt: phyletic history and ecological niche may constrainthe motor patterns that can be operantly conditioned, butthey never raise the possibility that the laws of thought mightbe species-specific.

These oversights are not inconsequential to a theory thatsets out to bridge the gap between motivation and behaviorand to explicate the organization of action. They reflect thefailure to come genuinely to terms with the ethologicalcritique of traditional experimental psychology. Ethologistsexperiment, but they experiment with behavior whose natu-ralistic context is known. They do not assume that theories ofbehavior are to be solely derived from isolated physiologicalpreparations confined to the laboratory bench. Gallistel'sbook, by failing to relate the physiological concepts to thelarger context of animal behavior, only tilts with ethologicalideas while consistently skirting the real methodologicalissues.

ACKNOWLEDGMENTThis work is produced by aid of a grant from the Harry FrankGuggenheim Foundation.

Gallistel's metatheory of action

H. L. RoitblatDepartment of Psychology, Columbia University, New York, N.Y. 10027

Gallistel's presentation of a "new synthesis" represents animportant contribution to our understanding of the factorsthat control behavior. It represents not so much a theory ofaction as a framework in which to cast such a theory. It is a"new way of seeing" (Kuhn 1962) behavioral phenomenaresulting from a modification of behaviorism.

One of the fundamental assumptions of behaviorism is thatof a direct correspondence between the overt features ofbehavior change - antecedent stimuli and resulting re-sponses - and the covert internal changes responsible forlearning. As Gallistel makes clear, this assumption allows onlya single level of organization, a direct connection between

stimuli and responses (S-R associations), itself having nointernal structure. This single-level control structure meansthat all behavior is controlled by reflexlike associations andthat all responses are elicited by external stimuli.

Gallistel replaces this assumption of external correspon-dence with a similar assumption of internal correspondenceinvolving at least three types of fundamental units - reflexes,oscillators, and servomechanisms - each under the control ofother elements arranged in a lattice hierarchy. In so doing, hehas solved a number of the most nagging problems confront-ing behaviorism. For example, the inclusion of endogenousoscillators removes any problem generated by the apparentspontaneity of behavior when external eliciting stimuli cannotbe identified. The relationship between motivation andperformance is solved through the inclusion of potentiationand depotentiation mechanisms that govern both motivationand performance. The problem of level of analysis in behav-ior - that is, the controversy over whether animals learnmuscle twitches or acts (operants) - is replaced by the hierar-chy principle according to which learning can take place atpractically any level.

Despite these innovations, Gallistel's synthesis is still only amodification of behaviorism. His strong commitment toreductionism and physical realizability permits nothing else.All of the principles and mechanisms that control behaviorreduce to interconnections among three fundamental units,sometimes augmented by apparently ad hoc modificationssuch as the autonomous buildup of specific potentiation.While this reductionism has shown itself to be quite powerfulin dealing with the organization of action at some levels,additional principles are undoubtedly necessary to deal withthe level of behavioral adaptation usually studies in thepsychological laboratory.

For example, the only mechanisms explicitly in the hierar-chy that could account for learning are the selective potentia-tion of reflexes and servomechanisms and the selectivecoupling of oscillators. Alone, these mechanisms do not consti-tute explanations. The task of any learning theory, whateverits scope, is to explain the particular changes that occur. Thehierarchy principle and its associated mechanisms are notsufficient to explain even the results of Wickens's (1939)finger-flexion experiment. Different subjects adapted to theexperimental demands at different levels of the hierarchy,one learning a particular reflex, the others learning an actionintegrated at a higher level.

The failure of Gallistel's synthesis as a theory of learningshould not be taken as a strong criticism of the system. It is notintended as a theory of learning, and in fact it is not even atheory of action. Examples of the hierarchy principle can befound ̂ everywhere. Because many actions involve the samesense organs and the same muscles with their innervatingneurons, the principle of a lattice hierarchy must be valid atsome level. Furthermore, practically any theory of action canbe described in terms compatible with a lattice hierarchy.Precisely this ubiquity prevents it from having explanatorypower.

A second problem (perhaps "lacuna" is a better term) is inGallistel's treatment of representations. It seems clear thatmuch of behavior is not easily describable in simple stimulus-response terms but seems to require the use of more elaboraterepresentations of knowledge. The question, then, is how thesystem that represents knowledge affects the system thatcontrols action.

Gallistel seems to attempt a solution to the problem byproposing two separate systems: a cognitive system, repre-senting knowledge, and an action system. On closer examina-tion, however, it becomes clear that these are really differentlevels in the same system. That is, Gallistel adopts the samesolution to the homunculus problem adopted by the behavior-ists, that of including knowledge as a part of the action


Commentary/GaWisteh Organization of action

system. His solution is a modification of the behavioristposition in that knowledge is assumed to be more complexthan simple changes in response propensities. The predictionof the behavior of an animal requires the specification of itsknowledge and its wants or goals. Callistel assumes thatmotivation spreads from goal-related motivational units highin the hierarchy through the map to selectively potentiateaction units at the level of telotaxes. Representations, likeother units of action, consist of interconnected nodes interact-ing with lower levels.

While unification of knowledge and action systems, likethe unification of motivation and action systems, has distinctadvantages, such as leading to articulatory coding schemes,the available evidence appears to demand more complexrepresentational systems containing dimensions orthogonal tothe action system (Roitblat 1980; 1981). Hulse & Dorsky(1979), for example, present quite strong evidence that ratsextract and represent information about a sequence of rein-forcer values that reflects the overall rule structure of thepattern. Learning is faster with monotonic than withnonmonotonic patterns, and there is a positive transfer fromone pattern to another employing the same rule. Despitearguments by Capaldi and his associates (Capaldi, Verry, &Davidson 1980) to the contrary, it is unlikely that this infor-mation could be stored in anything resembling an actionhierarchy. This point is further illustrated by the work on therotation of mental images done by Shepard and his associates(Shepard 1975; Cooper & Shepard 1979). Callistel recognizesthat the performance obtained with this task requires anelaboration of the hierarchical representational scheme toinclude dimensionally encoded vectors. Even this elaboration,however, is not sufficient to account for the finding thatgreater degrees of "mental rotation" take more time withoutthe ad hoc assumption that values in the dimensional vectorcan only be adjusted in a stepwise fashion. These experimentsappear to require a representational system that is orthogonalto the action system, not one "flowing" directly into it.

In summary, Callistel does present a new synthesis offar-reaching importance. Whatever difficulties are presentappear primarily to be the result of attempts to make thesystem operate as a theory of behavior. It is not a theory butmore of a metatheory, suggesting how theories of actionmight be organized and providing a framework in which tocast theories of behavior. It will certainly require elaboration,including more kinds of higher-level structures and the speci-fication of the particular laws that control the hierarchicalinteraction among units.

ACKNOWLEDGMENTPreparation of this manuscript was supported by NSF grant BNS7914212.

The education of behaviorism and the natureof learning

William TimberlakeDepartment of Psychology, Indiana University, Bloomington, Ind. 47401

The education of behaviorism. At last! Someone in themainstream of psychology has assembled in one book much ofthe historically important work on behavioral control, andattempted to integrate it into a general scheme that accountsfor current research. The result is a breath of fresh air forteachers and researchers trying to develop a more adequateconception of behavior than that provided by the reflex, theoperant, and neural pathways and centers. Most of us knew ofother conceptions, but reading in secondary sources abouttaxes, oscillators, servomechanisms, and hierarchical control

did no justice to the expository powers of the original writers,or to the background of their contributions. Most important,these different conceptions of the functional units of behaviorwere difficult to integrate into a common scheme. They werelargely based on unconnected pieces of research using (forpsychologists) peculiar subjects and procedures, and theresults were considered primarily relevant to issues of natureand nurture or to currently moot debates, such as whether thenervous system is spontaneously active.

Gallistel's great service was to point out the commonthemes in these classic works and to show how these themesare relevant to current research. There are arguable deficien-cies in this book. Not everyone will be pleased by his choice ofarticles, or by the inconsistent editing style. There wereimportant omissions, particularly in the analysis of organiza-tion of behavior at level 5 and above (e.g., McFarland 1974)and in his nearly exclusive focus on locomotion as an exampleof motor coordination and control. In addition, his conceptualframework will demand considerable work before it can betaken as adequate to account for current data. Gallistel's pointthat hierarchies are latticelike (that is, individual lower unitscan be controlled by many different higher units) is welltaken, but his illustrations from the military and businesssuggest that hierarchies are shaped like pyramids, with fewerand fewer units at each successive level. It seems to me thathierarchies in an animal are as often shaped like hourglasses,diamonds, or even upside-down pyramids.

Another point: though Gallistel treats reflexes, oscillators,and servomechanisms primarily as low-level units, they strikeme as representative functions and relations that are likely tobe found at both high and low levels of a hierarchy. Further, Isuspect that there are more complex units underlying behav-ior (Tinbergen 1951; Timberlake 1981), and that levels in ahierarchy may not be fixed but may actually reverse underdifferent circumstances. Last, any assumption of ascendinglevels of control culminating in the neocortex makes mesuspicious of a species bias. Gallistel's slightly cautious inter-pretation of the transection data provoked some wonder thatinvertebrates, even fish, reptiles, and birds, manage to getabout in an orderly fashion.

I doubt that Gallistel would disagree that his scheme isprovisional and incomplete. His attempt to include cognitivepsychology is suggestive of the potential of a general struc-tural approach, but it did not seem to me entirely successful.This may be more the fault of the dominant models incognitive psychology than of a flaw in his approach. What hehas shown is that we must treat behavior as an entity ofcomplex causation and control. In so doing we may be forcedto combine the varying conceptions underlying our researchinto a common final path, grounded in behavior but adequateto the complexities of information processing and decisonmaking.

The nature of learning. It may be fervently hoped that oneeffect of Gallistel's integration will be to drag our conceptionof learning into the twentieth century. Until recently, thestudy of animal learning has suffered gravely from an impov-erished model of the functioning organism, grounded in asimplistic and misinterpreted concept of the reflex that wascommon at the beginning of the twentieth century. (Gallis-tel's book is worth the price if only because it quotes enoughof Sherrington to show that a functioning reflex was not asimple automatic unit of behavior, but a complexly con-trolled, integrated, and adaptive entity.)

In most traditional studies of learning, an animal isassumed to bring to the test chamber only basic sensory andmotor equipment, a few reflexes, some regulatory tendencies,and its past learning. Even this simple equipment was deniedin part by those who attempted to reduce regulatory tenden-cies to an associative basis (Hull 1935; see Timberlake 1980),and reflexes to learning occurring in ontogeny (see Kuo 1967).


Response/Gallistel: Organization of action

Such oversimplification focused all attention on the hypothet-ical strengthening process that presumably intervenedbetween simple sensory reception and motor output toproduce learned behavior. This focus isolated the study oflearning from the animal's ecology (Timberlake 1981), itsregulatory processes (Timberlake 1980), and the physiologicalcoordination of its behavior.

In short, most of us have been studying learning usingpositivistic assertions that certain concepts exist (because wehave developed traditional methods for measuring them),combined with outmoded and incorrect reflex physiology (ormodels of learning derived from that physiology). It is time tomake the study of learning more continuous with the study ofmotor coordination and control. It is damaging to eachapproach to maintain sharp distinctions between them. Thephysiological units of motor coordination are vitally involvedin learned behavior, and in many cases learning is no lessinvolved in the control and integration of motor output. Theinvestigation of phenomena such as bird-song learning, withits clear intertwining of physiological mechanisms and learn-ing, may well be fundamental to the understanding of alllearning.

A potential contribution of researchers in learning may beto develop more complex models of the structures an animalbrings to the learning situation. I recently suggested such amodel to account for the behavior of two rodent speciestoward conspecifics that predicted food (Timberlake 1981).Within this model, low-level sensorimotor units (such asreflexes, taxes, and oscillators) are combined into larger unitsof perceptual-motor organization called modules. Eachmodule consists of responses that show statistical sequential/temporal relations and can be elicited, controlled, and termi-nated by particular stimuli. The modules are organized in aloosely hierarchical fashion into systems serving a commonfunction (such as the feeding system). Potentiation consists ofinput at the system level, and depotentiation depends on thenature and temporal relation of controlling stimuli.

Learning is presumed to occur within these systems in theform of modification of the frequency, order, timing, integra-tion, and elicitation of subunits, modules, and systems.Further, depending on the level and function, learning mayoccur as the result of response feedback, stimulus-responsepairing, motor repetition, or stimulus presentation. Theempirical realization of such a general model is a monumen-tal task. It may well be no more than a heuristic guide to othermodels. One hopes that Gallistel's timely integration willfacilitate the development of better models at the interfacebetween research in motor coordination, control, and learn-ing.

ACKNOWLEDGMENTI thank Connie Mueller for his conversation.

Author's Response

Matters of principle: Hierarchies,representations, and actionC. R. GallistelDepartment of Psychology. University of Pennsylvania, Philadelphia. Pa.19104

The two dominant themes in the BBS multiple reviewof my book are the adequacy of the principles I

propose for analyzing the action hierarchy and thenature of representations and how they are used by theaction system. I am glad that these themes dominate,because they are the dominant themes of the bookitself. I have grouped my responses under three head-ings: "Fundamental principles for analyzing the struc-ture of action," "Learning and representations," and"Miscellanea." Under "Miscellanea" come the more orless inevitable claims that nothing new has been saidand the equally inevitable complaints that I did not frysomeone else's favorite fish. Also included in this cate-gory are responses that primarily raise interesting andpertinent questions to which I have no good answer orthat voice sentiments with which I basically concur.

Fundamental principles for analyzing thestructure of action

Bolles. I agree that the essence of the hierarchicalnotion is that there are units capable of carrying outcertain functions on their own and then there aresuperordinate units that integrate these functions tocarry out more complex functions. The "autonomy" ofthe lower units, the fact that they have a structure thatenables them to execute certain operations (e.g., step-ping a leg) in the absence of any intervention fromabove, is of primary importance. This is why I aminclined to doubt the view that in the higher animalsevery kind of operation is carried out in the cortex (cf.Hollerbach). The kinds of "feedforward" or anticipa-tory correction mechanisms that Bolles calls attentionto in his hand-lifting example are clearly important. Idid not discuss these because I am not aware of anyprincipled analysis of how they are achieved. The fewdiscussions I have seen in the AI (artificial intelligence)literature strike me as ad hoc, contrived solely for thepurpose of explaining the example at hand, withoutany concern for generalizability or even testability.Perhaps, as Hollerbach seems to suggest, each schemeis unique to a particular case; if so, we are going to havea hard time creating our science. I am inclined to thinkthat there must be some generalizable principlesinvolved. The principles described by Dev seem to mevery promising.

Chappie. The questions Chappie raises are the kindsthat need to be asked again and again in the study ofbehavior. Is this particular piece of behavior anelementary or a complex unit of behavior? If elementa-ry, what kind of elementary unit? Are there elemen-tary units other than reflexes, oscillators, and servo-mechanisms? If so, what are their distinguishing char-acteristics? If we have to do with a complex unit, whatare its constituent units and how do they interrelate?

Let us take the so-called scratch "reflex" as anexample. Graham Brown (1910) showed that it has twoconstituents, a reflex raising of the paw to the point tobe scratched and an oscillatory scratching motion.Therefore the scratch "reflex" is not an elementaryunit of behavior. It is a complex unit, because it can beanalyzed into at least two constituents, each of whichhas the essential features of a unit of behavior -initiators (the sensory receptors that drive the reflex



positioning of the limb and the pacemaker that drivesthe rhythmic scratching), conductors, and effectors.Since the scratch "reflex" is not an elementary unit, itshould not be called a reflex, a name I would have usreserve for use in describing a particular kind ofelementary unit. This is the kind of principled analysisthat I think we should try to bring to the understandingof behavior.

Does one see examples of heterarchical organizationat lower levels? Probably, but I think that the general-ization that this kind of organization is more commonat higher levels is on safe ground. We will only besecure in making these kinds of generalizations whenwe have a great many very detailed analyses of behav-iors at all levels. Unless we strive always to make theseanalyses in terms of clearly stated principles, we willnot build a strong conceptual edifice. So, if there areother kinds of elementary units (and I do not doubt thatthere are), let us set about stating their distinguishingcharacteristics, as I have tried to do for the reflex, theservomechanism, and the oscillator. If there are otherimportant principles by which higher levels controllower levels (and I am sure there are), let us try to findconcrete examples of them, as I have tried to findconcrete examples of control by selective potentiationand depotentiation.

Craske. One of the main themes of the book is indeed acritique of those who think of behavior only in terms ofreflexes or only in terms of reflexes and voluntarybehavior, operant behavior, etc. I agree that Craske'sobservations suggest oscillators as significant compo-nents of everyday movements in humans. Had I beenaware of his work, I would have cited it.

Dev. As Dev no doubt knows, within any finite interval,a good approximation to an aperiodic trajectory maybe produced by a Fourier series that is not only finitebut in fact of modest length (<100 terms). However, Iam inclined to agree that aperiodic trajectories are notplanned in Fourier terms. (I am by no means confidentthat even periodic movements are planned in thisway.)

Dev's comments highlight an important concept thatI failed to cover in my book - namely, the idea that thecontrolled variable in many (maybe all) movements isthe set of length-tension curves for the muscles operat-ing on a joint. For any particular limb position, there isa family of sets of length-tension curves. Each memberof the family is a set of curves, one for each relevantmuscle. The intersection of the curves in a set yields thedesired position, subject to an error determined by theload. The family for a given position consists of allthose sets with the same intersection. The higher theaverage tension in a set belonging to this family, thegreater the stiffness of the limb, hence the less the errorproduced by any given load. The notion that the CNSselects a family based on the particular position itwants, and a set within the family based on the load itanticipates, goes a long way toward explaining how theCNS overcomes the nonlinear mechanical characteris-tics of limbs in realizing preplanned trajectories. Ibelieve it was Feldman (1966) who first advanced thisexplanation. The work of Bizzi, Dev, Morasso, & Polit

(1978) and others (e.g., Cooke 1979; Schmidt &McGown 1980) has provided experimental support forit. As Dev notes, this is a nonservo mode of control.

This length-tension (or mass-spring) theory of limbcontrol does not, however, address itself to the questionof how the to-be-executed trajectory is represented inthe first place. The question is, what is the mostnatural, economical "language" in which to formulatetrajectories? Perhaps most trajectories are specifiedsolely in terms of their end points, with the control ofdynamics being limited to the specification of stiffness.Or perhaps, as Dev suggests, selected aspects of thedynamics (e.g., peak velocity) are represented inadvance. In that case, any movement will be plannedin terms of a modest number of parameters. Obviously,we need experimental data on the question of theextent to which the dynamics of a movement aresubject to planned variation. If experiments shouldreveal that the complete time course of a movementmay be mapped out in advance, then -we will have toconfront the question: how does the CNS decomposearbitrary three-dimensional vector functions of timeinto a finite set of elementary functions, each having afinite set of parameters? One such decomposition isFourier decomposition. As Newell points out, there aremany others. For example, aperiodic movements couldbe planned in terms of a series of step functions.

Yet another question that remains to be addressed isthe one raised by Bolles. Most robots are anchored inthe upright position, but the animal body is not. Howdoes the CNS take account, in advance, of the effect ofan arbitrary limb displacement upon postural stability?Does it use a model of the body's biomechanics? On theface of it, such a model would be stupefyinglycomplex. Are there any simplifications possible? Isthere evidence that the CNS exploits these simplifica-tions? We are in no danger of running out of hardquestions anytime soon.

Doty. I am pleased that Doty finds the first and largestpart of my book congenial. I only wish I could convincehim and other neurophysiologically oriented physio-logical psychologists that abstract models with, for themoment, no neurophysiological content are not merenominalizations. Neurophysiology-free models areindispensable, both for understanding the behavioralphenomena and for understanding the neural basis ofthose phenomena. As late as the mid-1980s, A. V. Hillremained scrupulously agnostic as to the possiblephysio-chemical embodiment of excitation in nerves.He treated excitation as an abstract, physically myste-rious process. He used data from the nerve-musclepreparation to create a mathematical characterizationof this abstraction. The characterization did not specifythe physical nature of excitation, but it put strongconstraints on its possible embodiments (Hill 1932;1936). Similarly, the Hodgkin & Huxley model gives anonphysical treatment of the neuronal membrane, inthat it leaves the biophysics unspecified. What is thismystical talk about "gates"? the biophysicist is apt tosneer. But the Hodgkin & Huxley model is not so muchhot air; it is a very powerful theory, at its level ofanalysis.

To return to the example I used in the Precis, the



molecular genetics revolution is literally inconceivablein the absence of the conceptual framework providedby classical genetics. The possible molecular embodi-ment of the gene in classical genetics was at least asmysterious as is the possible neurophysiologicalembodiment of "a node representing food." But thatdid not make classical genetics a collection of emptywords papering over ignorance.

I think Deutsch's (1960) theory is wrong. My Fouriermodels probably are too. But they are not mere words.They give fairly explicit directions for constructing amachine that exhibits the phenomena that thesemodels seek to explain. The "principle of responsegeneralization" is, by contrast, a mere nominalization.This so-called principle gives no indication of how onewould build a machine that exhibited the phenomenathat Wickens (1938; 1939) found in his conditionedfinger withdrawal experiments, or any of the otherphenomena psychologists discuss under the heading"response generalization." The same is true for theprinciple of stimulus generalization and most of theother principles in the impoverished arsenal of S-Rpsychology.

Fentress. I think the kinds of worries Fentress hasabout the notion of units in behavior apply with equalforce to the units in other scientific areas. The atom,the proton, and the molecule are all units, but they arenone of them perfectly stable, nor indivisible, nor freefrom complex interactions with other units. That anatom is divisible into electrons, protons, and neutronsdoes not make it any the less a unit in scientificanalysis. That oxygen and hydrogen can combine toform water, a substance with properties markedlydifferent from those of hydrogen and oxygen, does notmean that hydrogen molecules and oxygen moleculesare not units in chemistry. That the radium atom is notstable does not make it any less a unit. Nor do thesecomplexities mean that one should abandon the notionof units in chemistry and physics and talk only ofprocess. Talk about a process is intelligible only whenone has well-defined units that enter into the process.None of this should be taken to mean, however, that Ithink that an adequate concept of the kinds of units wehave to deal with in behavior and the kinds of interac-tions these units enter into is easily arrived at. Theexamples Fentress gives nicely illustrate the kinds ofproblems we have to come to terms with.

Grillner. I am pleased that Crillner feels I haveadequately captured the general picture of movementcontrol held by those doing experimental work on themechanisms of movement. This was my primary goal.In retrospect, I see that the fatal word "new" in mytitle ought to have been left out. This bit of puffery onmy part clearly raised some hackles. The unstillablevoice of demon pride still whispers in my head that,while these ideas have been widely held, no one has putthem all together in one place in recent years, buildingfrom muscles to motivation and representation. Butenough of this vanity; indeed these ideas are commoncurrency, both within the experimental community,which I knew, and, it appears, within the artificial-intelligence community, which I had not realized. The

task now, as Crillner, Hollerbach, Lewis, and othersurge, is to look ahead to a lengthier and more reconditework that puts flesh on these bones, by focusing onmodern experimental work in this active and excitingfield.

Hogan. By raising Dawkins's (1976) distinctionbetween hierarchies of embedment and hierarchies ofconnection, Hogan brings an important issue into sharpfocus. I agree that at the behavioral level of analysis thesystem I describe is a hierarchy of embedment. Thestepping of an individual leg is embedded in walking.Walking is embedded in approaching food. Approach-ing food is embedded in nutritive behavior, and so on.What we find at the neural-circuit level of analysismay be viewed as either a hierarchy of connection or ahierarchy of embedment. There is an intraganglionicneural circuit whose function is to control the musclesthat cause an individual leg to step. This circuit can bemade to operate all by itself in the isolated hemigan-glion of a roach. Distinct from and superordinate to theintraganglionic leg-stepping circuits is the intergan-glionic circuitry whose function is to interrelate the sixleg-stepping circuits so that the legs step in a walkingpattern. This interganglionic circuitry carries out ahigher-level function. It does so by regulating theoperation of the intraganglionic leg-stepping circuits.The relation between the interganglionic andintraganglionic circuits is a hierarchy of connection.On the other hand, when we shift our attention to theneural circuitry that interrelates the operation of walk-ing circuitry and orienting circuitry to produceapproach, we may regard the walking circuitry as aunit, in which case the circuitry for stepping an indi-vidual leg is embedded in the walking circuitry. Inshort, intermediate units of behavior are not all at onelevel, as Hogan suggests. There are many levels. Inter-mediate units at higher levels have intermediate unitsat lower levels embedded in them, whether one choosesto work at a behavioral or at a neural-circuit level ofanalysis.

I agree that the pyramidal neuron route from thecortex directly to the motor neurons is not part of thediencephalon-dominated hierarchy that I have de-scribed. I suspect that this extrahierarchical route to themotor neurons is used by higher vertebrates for thekind of special-purpose direct-access programmingthat I allude to in my response to Hollerbach. Incomputers called on to perform special computations atgreat speed, the usual hierarchically structured high-level programming languages do not allow theprogrammer to write the most efficient program. Insuch cases, machine-language programmers are calledin to write a maximally efficient program in thelowest-level language. The pyramidal tract may be theagent of machine-language programming systems inthe cortex (another outrageous speculation, I fear).

There is no evidence that I know of that the wavingof a fish fin can be analyzed into constituents that areunits of behavior in their own right (whereas there issuch evidence for the scratch "reflex"; see my responseto Chappie). Until there is such evidence, this unitshould be regarded as an elementary unit of behavior,not a complex unit, which is what all units at Level 5



are. The same can be said for the vestibulo-ocularreflex, the optokinetic servomechanism, the flexionreflex, the proboscis extension reflex in the blowfly, theshort-latency tail-flip reflexes in the crayfish, andmany other examples. In short, I think there really areelementary units of behavior, and there really arecomplex units of behavior, and there are principledprocedures for telling which is which.

Hollerbach. This review raises a great many interestingpoints. I am afraid I have neither time nor space torespond adequately, but here goes.

Yes, I subscribe to Church's thesis.My description of oscillators, servomechanisms, and

reflexes is indeed coarse-grained and does not do justiceto the richness of the conceptual and methodologicalmaterial that one encounters upon delving more deeplyinto any of these topics. My choice of older, simplerpapers and a relatively simple level of discussion wasdetermined by the intention to provide students withan initial grasp of these entities and to give them someconcrete illustrations of how these units combine toproduce more complex behavior. I believe in the histo-rical approach to the understanding of major ideas,scientific or otherwise. Plunging students straight intothe latest work causes all but the best to lose the forestfor the trees. Modern work on servomechanisms makesheavy going for students who have largely forgottenwhatever calculus they may have learned. You have tomotivate their plunge into frequency domain analysis,integral control, predictive control, etc. by first givingthem some feel for how all this might add up to anunderstanding of behavior.

I am not sure what to make of the comments on theconcept of the reflex. They seem to imply that I regardoscillators and servomechanisms as reflexes, whereas Iwas at pains to distinguish them from reflexes. Thevestibulo-ocular reflex is a reflex. The optokinetic reac-tion is not a reflex; it is a servomechanism. The musclespindle system, if it in fact functioned as Merton (1973)imagined it might, would be a servomechanism; but, asHollerbach notes, it does not seem to function as aload-compensating servo. The long-loop compensationmechanisms now enjoying favor cannot be treated assimple servomechanisms, for just the reasons Holler-bach cites. That a reflex is subject to potentiation anddepotentiation from above does not make it any the lessa reflex. Sherrington knew better than anyone aboutthe potentiation and depotentiation of reflexes; heshowed the dramatic effects of various kinds of braintransections upon the elicitability of spinal reflexes.Sherrington's dualism, like Newton's theology, seems tohave had little impact on the essentials of his scientificthought. He did not think that these transectionsaffected the actions of the soul, although he apparentlydid think that any transection separated the neuralmachinery from the influence of the soul.

In my mind the jury is still out on how badfrequency domain (Fourier) theories are in vision andaudition. Are time and space domain theories notice-ably better? It seems to me that Hollerbach's (1981)own work on handwriting encourages one to think ofthe representation of these movements in Fourierterms; but I would be the first to admit that no

compelling case has yet been made.I agree that feedforward control is clearly important

(cf. Bolles), and I regret that I did not include somematerial on this in the book.

I think that the nervous system of advanced verte-brates has indeed found it necessary for some purposesto give very high levels direct access to very low levels.But I doubt that the already evolved intermediate unitsof coordination, which function well in most routinesituations and which need so little instruction fromabove, have been abandoned in favor of a system inwhich the cortex decides what every muscle is to bedoing at every moment.

I agree that the heterarchy-hierarchy distinction is arough cut, but a useful one nonetheless. By insisting onthe hierarchical character of the overall organization ofthe brain we remind ourselves that there are higher-level functions that are realized by the appropriatecontrol of lower-level functions. And we remindourselves that the behavioral consequences of an inter-vention, be it instruction, brain stimulation, lesions, orwhat have you, can only be understood if one has anidea of the level of functional integration at which theintervention produces an alteration. Knowing the leveldoes not make one's understanding in any waycomplete, but until one knows the level, understandinghas hardly begun. By acknowledging the presence ofheterarchical organization we remind ourselves not toforce everything into the hierarchical framework. Oneoften encounters modes of interaction that do not fitthe framework, and one has to be alert for them.However, I agree that as we acquire a better knowl-edge of the control structures that solve particularkinds of behavioral problems, we will need a muchricher set of categories for classifying these structures.Like Hollerbach and von Hoist, I think the attempt tounderstand behavior in terms of a very few primitiveshas been a failure. We have slit our throats withOccam's razor. However, I hope we do not now go tothe opposite extreme and imagine that the controlstructure for each piece of behavior is unique, workingby principles not found in any other control structure.Each structure may offer a unique combination ofprinciples. And some structures will prove to employunique principles. Most structures will prove to employprinciples also used in other structures, at least ifEinstein was right in assuming that God is subtle butnot malicious.

Jander. I am disappointed that my book has received soharsh an evaluation from a quarter where I hoped itmight find favor. Jander (1957) did seminal work onthe mechanism of menotaxis (for follow-ups, seeLinsenmair 1969; 1970; 1973). Franklin, Bell, &Jander's (in press) work on the leg movements made bythe cockroach in turning is an important new depar-ture in the analysis of the locomotory control structure.The works just cited are fine examples of the detailedbehavioral analysis of control and coordination mecha-nisms, the kind of detailed analysis that several review-ers call for and that I hope my book promotes. Suchanalyses are most useful when accompanied by acareful attention to principled distinctions. Jander'scriticisms give me occasion to reemphasize some of the


principled distinctions I make in my book.First, I used the term elementary units of behavior

advisedly because I explicitly include (not exclude, asJander recommends) the input side. I follow Sherring-ton in distinguishing between a unit of action, such asthe motor unit, which has no initiator (see Precis), anda unit of behavior, such as the reflex, which does. Sincemost units of behavior have a sensory/perceptualcomponent, it would be madness to build a theory ofaction on units that are in principle denied such acomponent. I defined my units in the way I didprecisely in order to avoid the inconsistency thatJander imputes to me.

I give explicit principles for distinguishing betweencomplex units and elementary units and for distin-guishing my three kinds of elementary units intomutually exclusive classes (see Precis for a recapitula-tion of these principles). The categories of elementaryunits, while mutually exclusive, are not exhaustive,because I think there are other classes yet to be defined.I do not think there are only three classes of elementaryunits and I explicitly say so (Organization of Action,henceforth Action, p. 210). Reflexes are common, andthey are not servomechanisms or parts of servomecha-nisms. The vestibulo-ocular reflex, saccadic eye-orient-ing reflexes, and the flexion reflex to painful pawstimuli are a few among innumerable possible exam-ples of elementary units of behavior that are reflexesand not servomechanisms. Some units that are some-times called reflexes in common parlance are in factservomechanisms (e.g., the optokinetic reflex, which Iam careful to call the optokinetic reaction). I hope thatmy book will serve to correct some of these inaccura-cies in common parlance by focusing attention on theneed for a principled terminology.

The feedback component is irrelevant in saccadiceye-orienting movements because altering the feed-back during the course of the movement has no effecton the course of the movement. Ditto for the flexionreflex. This is the principle by which one distinguishesreflexes from servomechanisms in the many caseswhere the possibility of servomechanistic feedbackexists. I clearly state this principle in Action (p. 145).Where is the arbitrariness in any of this? This is atextbook prescription for distinguishing servo controlfrom nonservo control: open any loops and see if thatmatters.

If my principles are adhered to, there is no danger ofclassifying feeding behavior as a servomechanism,because feeding behavior is obviously a complex unit ofbehavior. The term "servomechanism" applies only toelementary units. There are, of course, servomechanis-tic aspects to the control of feeding behavior, as I pointout in chapter 10, but the theory of simple servomech-anisms is transparently inadequate to capture these.The scratch "reflex" is indeed a complex unit ofbehavior, one of whose constituents is an oscillator (seemy response to Chappie). Again, if my principles areadhered to, there is no danger of misclassifying thisunit.

I tried to adhere to the distinction between anoscillator, which is a unit of behavior, and a pacemak-er, which is the autonomously active neural element orcircuit that serves as the initiator constituent of an


oscillator. I may have slipped up on this in one or twoplaces; if so, I am sorry.

My use of "taxis" generally follows Fraenkel &Gunn's (1961) distinction between the orienting mech-anism (the taxis proper) and the locomotory mecha-nism, whose operation may or may not accompany theoperation of the orienting mechanism. The violation ofthis usage in Action, p. 275, is implicit, not explicit. Itoccurs in a passage that refers back to Fraenkel's paper(reprinted in chapter 6), a fifty-year-old paper inwhich this distinction was not made. Jander's going tothis length to find fault seems to me a little bizarre. Thesame applies to his criticism of my definition of anelementary unit of behavior in the Glossary. Janderomits from his quote the next sentence of the defini-tion, which begins, "It [the circuit] must have a compo-nent or components in which nerve signals arise. . . . "That makes clear provision for the sensory receptors inreflexes and servomechanisms, a point on which Icannot imagine anyone reading my book being in anydoubt. The fault Jander finds here would seem to applyonly if one follows his (not my) proposal to disregardreception, perception, and cognition in building ahierarchic system of concepts to describe action.

At several places in my book I call attention to thefact that the lattice-hierarchical arrangement requiresintralevel mechanisms that decide which of the manycompeting units actually has control over lower-levelunits at any one time. In my discussion of recurrentreciprocal inhibition (Action, pp. 60-63), I discuss onesuch mechanism at length. How I can be accused ofignoring this problem baffles me. To say that thisproblem falsifies the lattice-hierarchy theory does notmake sense.

I find the remarks on my Fourier models incompre-hensible. The magnet effect, far from being inconsis-tent with such models, may be invoked to explain howthe oscillators maintain the proper phase relationshipwhen the pattern is executed. That some processes inthe nervous system are nonlinear does not mean thatthey all are.

I agree that data on navigation after detours requirea theory of spatial representation different fromDeutsch's, and I say so in the book.

I propose calling the framework espoused in mybook "the neuroethological theory of action (in recog-nition of its roots in behavioral neurobiology and ethol-ogy)" [Action, p. 361]. I pay a great deal of attention tothe work of von Hoist, Lorenz, and Tinbergen. I cannotimagine why Jander seems to feel that I follow thepsychologists' long tradition of ignoring or rejectingethological theories. On the contrary, I like to think ofmy book as a modern synthesis of the ethologicalposition on the structure of behavior. Mittelstaedt haswritten to me that he plans to respond to my critics in alater round in this journal, rather than writing anythingfor this round. It will be interesting to read his responseto Jander, since Mittelstaedt writes from the citadel atSeewiesen.

Jeannerod. I find myself in agreement with Jeannerodand with the point made by his interesting experiment.His arguments illustrate the futility of attempting tobuild a theory of action with units that are denied an



input component. Rather than banning input fromconsideration, as Jander recommends, I ought to havedevoted more attention to it, as Jeannerod recom-mends.

Lewis. I agree that dynamic considerations are centralto understanding how sophisticated servomechanismsreally work. I mention in my Precis (but not in thebook) the fact that stability considerations require apoor high-frequency response in the optokinetic reac-tion. I heartily second Lewis's recommendation thatthe serious student delve into more recent literature,where much more sophisticated treatments of servo-mechanisms are to be found (e.g., Baarsma & Collewijn1974; Carpenter 1977; Crago, Houk, & Hasan 1976).The student who does so should be forewarned, howev-er, that a working knowledge of linear systems theory isessential (see Caelli 1981; Carpenter's Appendix;Norman 1981; and Riggs 1970, for biologically orpsychologically oriented introductions to linear systemstheory).

Nashner. I am pleased that Nashner finds my exposi-tion of the principles of motor organization congenial. Ithink his own work provides excellent examples oflearned selective potentiation and depotentiation atwork in human motor control (Nashner, Woollacott, &Tuma 1979). I regret that I became aware of his worktoo late to include some of these examples in the book.

Learning and representations

MacKay. I agree that I slighted Lashley, but notbecause I don't admire him. His work just did nothappen to fit conveniently into the exposition. I do,however, explicitly acknowledge his early advance-ment of the selective-potentiation view of motivation.Also, his work is very well known to psychologists. I wastrying mostly to bring together less well known workpertinent to some of the problems Lashley highlighted,though not, I admit, to problems of morpheme andphoneme sequencing in speech or to the problem offinger sequencing in the playing of an instrument(classic problems in the serial order of behavior, aboutwhich I simply have nothing interesting to say). I alsoconcur with MacKay's argument that an abstractmuscle-independent representation of learned move-ments such as handwriting is not the whole story. Theremust indeed be effects of experience at other levels,effects that have a considerable bearing on the fluidityand precision of the process that translates the muscle-independent representation into muscular expression.In my desire to show that one could give a concreteneurobiologically plausible model of the abstract repre-sentation, I did not emphasize enough the importanceof plastic alterations at lower levels of the hierarchy.MacKay and I are one in believing that plasticity andlearning cannot be intelligibly discussed without takinginto account the different levels of the hierarchy andthe differing functional consequences of plastic altera-tions at different levels.

Mackintosh. I do not see my notions of learning as

falling within the classical-conditioning framework, aconceptual edifice about which I am skeptical. In myheart of hearts I do not believe that the process ofclassical conditioning, as traditionally conceived, everoccurs; nor, for that matter, does the process of instru-mental conditioning. I think the classic conceptions ofthe processes underlying these experimental phenom-ena are simply wrong. If we relax our conception ofclassical conditioning to the point where it refers to thelearning of any stimulus relation, no matter what therelation, no matter what the mode of representing thatrelation, and no matter what the procedures for trans-lating the representation into action, then of course theconception applies. But, in this relaxed form, the "theo-ry" of classical conditioning begs all of the interestingquestions. It disguises rather than highlights the diver-sity of plastic phenomena. It avoids raising all of thedifficult questions about the nature of representations(see Miiner and Reed). It takes no account of thedifferent levels of organization and the differing conse-quences of alterations at each level (see MacKay).

Miiner. Since in Miiner's case my critic directs his firstfire at von Hoist and Mittelstaedt's paper, I'll leave thereturn salvo largely to Mittelstaedt (who, as Imentioned, has written me that he plans to respond tomy critics in a later round). I note only the following:von Hoist and Mittelstaedt do not pretend to offer acomplete theory of movement perception. Perceptionsof movement in train stations seem to me irrelevant tothe issue of how false reafferent movement signals aredealt with. Despite our extensive experience that build-ings and trees don't move, the reader can easily verifythe fact that when you push on your eyeball with yourfinger, the whole visual scene, including trees andhouses, does seem to move. And the whole visual sceneis seen to move by subjects who attempt to move theireyes voluntarily when they have a drug- or disease-induced debility in the peripheral neuromuscularapparatus for eye movement. Together, these twoobservations seem to me strongly to imply the opera-tion of a mechanism that algebraically cancels reaffer-ent visual-field-motion signals with a copy of the signalthat normally commands eye movement. As regardsour realizing that something is no longer in the line ofgaze after an eye movement, this objection presumesthat perceptions of movement are not mediated by aseparate channel from perceptions of spatial locus;whereas there are both behavioral and neurophysiolog-ical reasons for believing that these percepts arehandled by separate channels.

I think it is highly unlikely that our movementsthrough space are directed by a code that explicitlyspecifies the outcome of each motor performance.Naturalistic observations by Calhoun (1963), the exper-iments by Maier (1929) and Thorpe (1950) reviewed inmy book, and a great deal of material reviewed byO'Keefe & Nadel (1978) [See BBS 2(4) 1979] show thatanimals are capable of taking a direct route from anypoint in a familiar environment to any other. Thedigger wasp transported to an arbitrary point finds itsway to its unseeable burrow. The triggered motorprogram (S-R) view advocated by Miiner requires aninfinite number of learned programs and even then


cannot explain how the animal sets an appropriatehomeward course from a point it has never been to.Setting a course from a point where one has never beentoward a home (or other goal) that gives off no stimulusbeacon detectable at a distance requires reference tolandmarks that define a spatial locus for both the goaland the starting position. This reference presupposes amap that localizes the goal in a space defined bylandmarks, at least some of which are detectable fromthe starting point of the course. The only possiblealternative I am familiar with - inertial navigation -relies on double integration of the acceleration vector.Since the capacity to find one's way home withoutrelying on beacons or trails seems very widespread inthe animal kingdom (cf. Jander), I believe that theability to make and use spatial representations isequally widespread. Either that, or animals have iner-tial navigation mechanisms of heretofore undreamed-of precision.

It is true that Deutsch's theory offers no clear indica-tion of how nonspatial representations might be trans-lated into appropriate actions. I think his theory isinadequate to deal with even spatial representations(though it is useful for illustrative purposes, as Milnernotes). However, I think a more adequate theory willbe even more peculiarly spatial. I think the quest for ageneral theory of learning of the kind Milner wants is awill-o'-the-wisp that has sidetracked psychology formost of this century. There are, I believe, many distinctorgans for learning in the brain [cf. Chomsky: "Rulesand Representations" BBS 3(1) 1980], each prepared tolearn about quite different aspects of reality. There areequally as many readout systems for translating whathas been learned into action. The organ (braincircuitry) that learns where things are is, I believe, bothfunctionally and morphologically distinct from theorgan that learns what causes what. And the systemthat translates spatial knowledge into action is likewisedistinct from the system that translates causal knowl-edge into action, although both systems undoubtedlyemploy the same hierarchically organized units ofaction. This pretheoretical bias about the nature oflearning and representations raises several perplexingquestions:

1. What are the fundamental modes of representa-tion? For many years most psychologists have assumedthat there was one and only one fundamental mode ofrepresentation, a representation in terms of associa-tions. I am inclined to believe that this mode ofrepresentation never occurs. I am inclined to argue thatan association, as classically conceived, never forms inthe brain of any animal, man included. What do form,I would assume, are among other things, representa-tions of spatial locus. These representations of spatiallocus could themselves be represented in a formalpsychological theory by sets of Cartesian coordinates.In short, I believe the brain literally makes maps. Butformal systems suitable for representing spatial primi-tives (points, lines, etc.) appear hopelessly ill suited torepresent other aspects of reality, such as causation.Therefore, I must assume that there are other equallyfundamental modes of representation in the brain.What are they? Good question.

2. How do we decide whether a proposed mode of


representation really does exist in the brain? I havenothing to add to what Chomsky (1980) had to say onthis difficult question in the pages of this journal. Wecannot decide a priori. We decide ultimately on thebasis of how coherent and powerful the various propos-als prove to be when confronted with an array ofexperimental and observational facts.

3. Within a mode of representation, what is repre-sented explicitly and what is derived from the directlyrepresented information when the occasion demands?This is the question most directly at issue in Milner'sand my opposing views about the nature of the repre-sentation underlying navigational competence. Milnerassumes that the animal explicitly represents the factthat proceeding X meters from A at an angle a to theline AB leads to the appearance of C; Reed seems tothink that this is what I assume. On the contrary, Iassume that the animal represents explicitly only thecoordinates of A, B, and C within some common spatialframe of reference. From these coordinates the animalderives the required angle and distance of progressionwhen and if the occasion demands. How does onedecide who is right? By the kinds of arguments givenabove, I think. My proposal explains how animals canderive a course from an arbitrary, previously unvisitedpoint, provided only that they are given sensory infor-mation that enables them to determine the coordinatesof that point within the common frame of reference.Milner's proposal, so far as I can see, cannot explain theability to set a correct course from an arbitrary point, apoint never visited before (assuming always that thepoint toward which the course is set is not the source ofany sensory information at the time the course is set). Ifexperiments confirm that animals can in fact do this,then the Cartesian-coordinates proposal has more meritthan the act-outcome proposal.

Reed. I agree that most, perhaps all, of the ideas in mybook are not new. Many can no doubt be found in someform in the writings of the ancients, just as can thegerms of the atomic theory of matter. I think whatcounts in science is not the propounding of an idea butthe marshalling of a compelling body of facts andarguments in support of an idea. By the way, didDescartes really say that the cognitive machinery selec-tively potentiates the machinery of the body? He saidthe soul directs the machinery of the body, but did hesay it selectively potentiates it? I'm no Descartes schol-ar, but it doesn't sound like him. In any case, that is notwhat what I say. I say that selective potentiation by amotivational signal of points in a representation deter-mines which external stimulus will be oriented to.

The problem of how representations are translatedinto action is indeed a vexing one, and I make no claimsto have solved it. I object, however, to the characteriza-tion of my speculations about the neural mechanismsunderlying the brain's representation of spatial config-urations as vague and desultory. As explained in thePrecis - [not seen by reviewers; ed.] - as well as in thebook, the idea is that the distribution of matter inthree-dimensional space could be represented in thefrequency domain; that is, the brain could use signalvectors specifying the frequencies, amplitudes, phases,and orientations of Fourier components. If the repre-



sentation does take this form, then it could be rotatedby changing the values of the phase and orientationsignals in each vector. Such a rotation would neces-sarily be continuous. These suggestions are speculativein the extreme, "outrageous" even (cf. Hogan), but notvague. Nor are they desultory in a discussion of howthe brain might form spatial representations and utilizethem in the control of action.

I agree that proposals about spatial representationsshould be designed to generate tests and explain facts.Kenneth Cheng and I are working on a combinedformal and experimental analysis of the hypothesis thatrats utilize a Euclidean representation of their environ-ment in finding their way about in the dark (see alsoLandau, Gleitman, & Spelke, in press). There are,however, some experimental facts already at hand,facts that badly want explanation. One such fact is thatdigger wasps, who make a visual survey of their newlydug burrow, can use the results of this survey to findtheir way home from any location within about 100meters away, even from never-visited locations towhich they have been transported inside a closed box(Thorpe 1950). Since there is compelling evidence thatthe burrow itself gives off no stimulus beacon detect-able even a meter away (Tinbergen & Kruyt 1938), Iknow of only two possible explanations: the wasps (1)use a map made during their visual survey, or (2) carryout nearly perfect double integration of the accelera-tion vector over the better part of an hour while movedthis way and that over hundreds of meters, both by.their own efforts and by the whim of the experimenter.I favor the first of these two explanations. If Reed (oranyone else) knows of an alternative explanation, or ofany reason to believe that such a feat of double integra-tion is remotely conceivable, then I am genuinelyanxious to learn of it. (Solar navigation belongs in themap class, since to find its way home from an arbitrarypoint using the sun as a reference the animal mustknow the latitude and longitude of its burrow - andhave a wondrously good clock and an astonishinglyprecise system for shooting the sun.)

Which brings me to counterfactual conditionals anddiving gannets. The reader should know that my booksays absolutely nothing about either of these topics. Iwould not dream of suggesting that the gannet gener-ates the appropriate wing retractions through theagency of a counterfactual conditional. Like Lee(1980), I assume the retraction is triggered by someaspect of the expanding optical array. How this mecha-nism has evolved I do not pretend to guess. Thefanciful evolutionary reasoning in which Reedindulges on this subject strikes me as the sort of thingthat has given evolutionary reasoning a bad name, abad name much resented by those who make moredisciplined evolutionary arguments.

Do representations go beyond the informationgiven? Yes; if they did not, they would be of little use.Chomsky (1980) has made this argument better than Ican (his "poverty of the stimulus" argument andaccompanying references). Let me illustrate, in thespatial domain, why representations must go beyondthe information given. A blind girl led from A to B andback to A, then from A to C, can apparently computethe approximate angle and distance she must go to

reach B from C (Landau et al., in press). The systemunderlying her movements through space seems toemploy trigonometric calculations, with the sensorydata obtained on earlier routes used to compute thenew route. Sensory data about the distances AC and ABand the angle BAC would make the calculation of thedistance CB and the angle ACB possible only if inrepresenting these data the brain assumes that theroom is a Euclidean space. If the space were assumed tobe Riemannian, there would be no way to calculate therequired distances and angles in the absence of infor-mation about the local curvature of space. Of course,the space is in fact Riemannian, although the curvatureis so weak that the space departs by immeasurablysmall amounts from the Euclidean within the confinesof the room. The point is that if the child's system forspatial representation were to adopt an agnostic stancevis-a-vis the Euclidean or non-Euclidean character ofthe space, it would not be able to support the requisitecalculations, calculations whose biological utility for ablind child (or a rat in the dark) is tolerably obvious.

Roitblat. It will come as startling news to Chomsky(1980) that a strong commitment to reductionism andphysical realizability permits nothing but a modifiedbehaviorism. Chomsky is strongly committed to reduc-tionism and physical realizability. If his theories are butmodified behaviorism, then behaviorism is moreprotean than was heretofore suspected.

I agree that I do not attempt to specify conditionsunder which learning will occur at one or another levelof the hierarchy. My views on the disparate characterof different kinds of learning preclude any generalattack on this problem. They argue instead fordomain-specific analyses. Since there is a lot of discus-sion of representations in the last chapter of my book,and since the laying down of representations underliesmany kinds of learning, it is erroneous to say that theonly mechanisms that could account for learning arethe selective potentiation of reflexes and servomecha-nisms and the selective coupling of oscillators. Thelaying down of a spatial representation has nothing todo with servomechanisms, oscillators, or reflexes, and Ido not see how these maps can be viewed as "stored in. . . an action hierarchy." Like Roitblat, I think repre-sentational systems are largely orthogonal to the sensor-imotor system. Of course, the sensorimotor system musthave access to the represented information; otherwisethere is no point to the brain's representing informationin the first place. Does any theory that grants the actionsystem access to the representation include the knowl-edge "as part of the action system"? If so, then thelibrary at my university must be seen as part of myaction system, as must the road maps I use in driving tounfamiliar places.

In any decompositional representation of space thathas orientation information directly represented bydistinct signals, rotation of the representation will takeplace by changing the strengths of those signals. It ishardly ad hoc to assume that those changes will becontinuous; most signals change strength continuously.

Timberlake. After hearing from the AI fraternity thateverything in my book is old hat, it is pleasant to find



that someone thinks that the synthesis at least is new,which is the farthest I would go in claiming originali-ty-

As regards the supposedly pyramidal shape of myhierarchy, see the section on oligarchs in the Precis.

In chapter 10, I explicitly call attention to theservomechanistic, oscillatory, and reflexlike characterof some of the processes at the top of the hierarchy.But, as explained in my response to Jander, one mustbe careful to avoid saying that these complex units atthe top are servomechanisms, reflexes, or oscillators. Tosay that they are is a little like saying that an organicacid is a hydrogen ion just because it is a proton donor.Any acid has some of the characteristics of the hydro-gen ion, but if we start calling all acids hydrogen ions,nothing but confusion will result.

I do not think I mention the neocortex anywhere inmy book. For me, the hypothalamus and the forebrainstructures with which it is immediately connectedconstitute the top of the action hierarchy. Although Ido not say so in the book, I imagine that corticalstructures are used primarily for analysis, representa-tion, and planning, and perhaps also for special-purpose interventions in very-low-level operations (cf.response to Hogan). Therefore I am hardly baffled bythe ability of fish, reptiles, and birds to get through life.They all have well-developed diencephalons and,evidently, enough forebrain to handle their morelimited analysis and planning problems. The vertebratedivisions of the brain, of course, do not apply toinvertebrates, but in invertebrates it is clear that higherganglia subserve higher functions, just as in vertebrates.A cockroach with its head cut off can run, but not toany clear purpose.

Needless to say, in the light of the many remarks Ihave already made on the topic, I concur with Timber-lake's criticism of the traditional approaches to learn-ing, which ignore the hierarchical structure ofbehavior, and which assume that the concept of anassociation is adequate to deal with the phenomena oflearning. The chorus of voices singing that there are nogeneral laws of learning grows louder all the time. Tomy ears, it is a chorus of angels.

Miscellanea

Arbib. Arbib and I clearly have different tastes. Sincehe does not say what important concepts I missed in thework he wishes I had dealt with, there is little more tosay. Maybe the AI people have known all this all along.If so, they have not, so far as I know, applied it to thekinds of problems in animal behavior that interest me. Idid not pay more attention to Greene's work becausethe few papers I read struck me the way much work inartificial intelligence does - very abstract and sche-matic with little attention to concrete examples drawnfrom the experimental literature. I thank Arbib forcalling Stelmach & Requin (1980) to my attention. Ihave not had time to look at it yet; but I will. I was also,I blush to confess, unaware of Arbib & Lieblich (1977).It sounds as though this article does tackle the kinds of

problems in animal behavior that interest me, and I amanxious to see what it has to say.

Newell. I agree that many of the notions upon whichmy argument is built have had some currency for along time, particularly the notion of control by selec-tive potentiation and depotentiation (which Reedtraces back to Descartes). I see my contribution here as(1) providing concrete examples of the operation ofthese principles; (2) emphasizing the diversity of prin-ciples needed - instead of, like Hebb, trying to make asingle, basically associationist concept do all the work;and (3) calling attention to the importance of somesystems (e.g., systems of coupled oscillators) that haveescaped the attention of many. While the term "hand-wave" makes me bridle a little, I heartily agree thatmore detailed discussion is needed on every topic. Ihope the book gives students their bearings before theyplunge into more detailed analyses. The questionsraised in Newell's penultimate paragraph are all perti-nent. I hope the book may help focus attention onthem. The Fourier models are put forward to illustratethe potential benefits of nonobvious decompositionalrepresentations. Other types of decomposition mayturn out to be preferable.

Olton. The question raised by Olton - why animalssometimes make intelligent use of their representationsand sometimes do not - is an interesting one. I amafraid I have no answer. The fact that by appropriatemanipulations one can make all but the highest animalsbehave as if they have no representations at all hashelped keep radical behaviorism alive into the fourthquarter of the twentieth century. The problem ofmaintaining tight experimental control while at thesame time arranging matters so that rats make full useof their spatial representations is one that KennethCheng and I are contending with right now. We wishthat we had some clear, readily articulable, andconvincing answers to Olton's thoughtful question. Allwe have at the moment are hunches.

Provine. I agree that the theory of the response hasbeen sadly neglected in psychology. Provine is perhapsas surprised as I am to learn from Arbib and Newellthat the artificial intelligence community has had atheory of animal action much like the one in my bookfor all these years. If my book succeeds, howeverunwittingly, in popularizing within psychology the AItheory of animal action, then experimentalists likeProvine, who do fine work on motor systems, will notfeel all alone in the wilderness any more.

Reynolds. What I wrote about were the mechanismsand principles underlying the patterning of muscularcontractions into complex purposive behavior. I agreethat I did not cover social behavior, ecology, communi-cation, the evolution of behavior, or species-specificityin the laws of thought. I also neglected quantummechanics, the fragmentation of genes in eukaryoticDNA, the rise of the aristocracy in the Middle Ages, thelamentable irrationality of the V2, and the transcen-dence of ir - capital subjects, every one.


References/Gallistel: Organization of action

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Gallistel 1981 - Organization of Action