Encyclopedia of Neuroscience || Central Pattern Generators: Sensory Feedback

Central Pattern Generators: Sensory Feedback 701

Central Pattern Generators: Sensory Feedback
W O Friesen, University of Virginia, Charlottesville,VA, USA
ã 2009 Elsevier Ltd. All rights reserved.

Introduction

Originating near the beginning of the twentieth cen-tury, two seemingly incompatible theories informedmuch of the debate concerning the neural origins ofrhythmic movements in animals. One theory, putforth most clearly by Charles Sherrington, held thatlocomotory patterns, although coordinated by thecentral nervous system (CNS), arise from sensoryfeedback and reflexes. Although counterexampleswere offered by several investigators, this theory waswidely accepted before the 1960s. The second theory,ably proposed by T Graham Brown, held that centralpattern generators (CPGs) formed by inhibitory neu-ronal circuits within the CNS are the source of rhyth-mic movement patterns. The latter theory gainedrenewed support from the work of Donald Wilsonon locust flight in 1961 and finally became dogmaduring subsequent decades as more and more CPGcircuits were identified in both vertebrates and inver-tebrates. Near the end of the twentieth century, theimportance of sensory feedback for the expression ofefficient locomotion received new recognition, lead-ing to a convergence of the two theories. The consen-sus is that the neuronal circuits underlying locomotioncomprise a distributed system that includes both cen-tral oscillators and sensory feedback components.The reemerging recognition that sensory feedback

plays an essential role in animal locomotion (andother rhythmic movements) includes the realizationthat sensory neurons exhibit many of the character-istics that define elements of a CPG. Thus it has nowbeen demonstrated that sensory neurons (1) expressrhythmic activity during locomotion, (2) make synap-tic contacts with CPG interneurons, and (3) canentrain the CPG when they are stimulated rhythmi-cally. Systems that provide examples of these charac-teristics include locust flight, swimming in leechesand lamprey, crayfish swimmeret beating, and walk-ing in stick insects and crayfish.

What Is Sensory Feedback?

The neuronal activity patterns that underlie rhythmicmovements in a wide variety of animal species aregenerated by complex neuronal circuits, the CPGs,located within the CNS. In addition, a multitude ofsensory receptors, found in the joints, muscles, and

other structures of the periphery, detect internal jointpositions and movements as well as environmentalfactors. The overt movements that constitute animalbehavior arise from the interplay between the CPGsand sensory feedback from these body structures.Because animals live in environments that are char-acterized by both temporal change and spatial unpre-dictability, the instinctive, inherited CPG controlcircuits cannot be expected to, and do not in fact,generate movement patterns that ensure adaptivebehavior. Consequently, CPGs underlying all animalmovements are subject to inputs via receptors thatmonitor the execution of motor commands in rela-tionship to the environment and then provide inputsto motor neurons and to the central neuronal circuitsthat form the essential core of CPGs. Such inputsmodify the neuronal activity patterns arising fromthe CPG with critical effects on movement amplitude,phase relationships, and the cycle period (or, equiva-lently, the frequency) of movements. The focus here ison the relationship of CPGs and sensory feedback in afew well-studied invertebrates and a primitive fish,the lamprey. A schematic overview of one such sys-tem, which controls the swimming movement in themedicinal leech, illustrates the general properties ofthe interactions between CPGs, motor output, andsensory feedback (Figure 1).

Why CPGs Are Subject to Sensory Feedback

In many animal preparations, the output of the CPGcan be observed in greatly reduced preparations,which often include only parts of the CNS. Compar-isons of CPG neuronal motor output with activitypatterns observed in intact, behaving animals providethe basis for the concept of a CPG, and, more ger-mane here, the comparisons have revealed deficits inmotor patterns that arise when sensory feedback isabsent. Most prominent, and most important, amongsuch deficits are that neuronal activity patterns gen-erated by CPGs in isolation have increased cycle per-iods, reduced activity amplitudes and suboptimalphase relationships. Moreover, in the absence of sen-sory cues, or internal changes in state, motor outputtends to represent rather simple movements, such asstraight-ahead locomotion, rather than the morecomplex movements observed in the intact animal.

Unpredictable development There are numerousfactors that mandate sensory feedback if animals areto behave adaptively, including body growth duringdevelopment and maturation. Amplitude and fre-quency of movements alter with growth; hence, onemajor consideration is the matching of CPG output to

Body-wall movement

Body-wall movement

Stretchreceptorinput

Stretchreceptorinput

Motoroutput

Motoroutput

Posteriorganglion

Anteriorganglion

Longitudinalmuscle

Longitudinalmuscle

SR

SR

Figure 1 Schematic model for the neuronal control of swimming

in the leech. Two segmental central pattern generators (CPGs)

within ventral nerve cord ganglia are represented by unit oscilla-

tors ( �). These unit oscillators are interconnected and mutually

entrained by intersegmental axons that run through nerve cord

connectives. The cycle period of the CPG is greater than in the

intact animal, whereas intersegmental phase lags are smaller.

Segmental motor neurons driven by the CPGs control muscle

contraction in their individual segments (red arrows from CPG).

When swimming movements are generated by the intact animal,

tensions in the body wall, arising from local motor neuron output,

mechanical coupling between body wall segments (dashed

arrows), and the environment provide sensory feedback (blue

arrows) to the CPG. This rhythmic input acts to decrease cycle

period and to increase intersegmental phase lags in the intact

leech. Symbols: SR, stretch receptor; �, CPG. Reprinted from

Yu X and Friesen WO (2004) Entrainment of leech swimming

activity by the ventral stretch receptor. Journal of Comparative

Physiology 190: 939–949, figure 6, ã 2004 Springer-Verlag, withkind permission of Springer Science and Business Media.

702 Central Pattern Generators: Sensory Feedback

the natural, resonant frequen cy of limb or body.Although develop ment changes in the CPG and thebody struc ture may be coordi nately regulate d bygenet ics, mat uration pro cesses depend also on theenviro nment. With the latter not fully predictabl e,sensor y feedba ck that modi fies CPG freque ncy,phase, and amplitu de provide s a means of ensuri ngthat body movem ents are efficient at all stages ofgrow th.

Unpredic table environme nt Animal s live in a widevariety of hab itats. Some, like fish or fly ing insects andbirds , move in nearl y homo geneous medi a; neverthe-less, obstac les, turbul ence, or tem peratu re clines areunpred ictable, setting up the esse ntial requi rement forsensor y input to the CPG, even for swimmin g andflight . Terrestr ial environ ments exhibi t a very highdegree of unpr edictabi lity; hence it is not surprisi ngthat CPGs underl ying walking and stepping are evenmore strongly controll ed by sensor y inputs .

Compensat ion for morphol ogica l alt erations Fur-ther requi rements for sensor y feedba ck arise fromalterat ions in an animal’s form through feeding, acci-dent, or predat ion. A pa rticularl y telli ng ex amplecome s from walking locomotio n in inse cts, whi chmodi fy their gait immediat ely when a leg is experi-menta lly amput ated. Other examples incl ude sea-sonal siz e and weight alterat ions that requi re areprogr amming of the motor system but cannot beexpect ed to alter the CPG . Althou gh hormone s canreprogr am the ne rvous system to match an an imal’sactivi ty to its ov erall con dition, only sensory feed-back can provide cycle-by -cycle feedba ck from theenviro nment.

Components of Motor Systems

Mo tor syst ems, whet her gen erating the neuron al sub-strates of locomo tion or other rhythmic movem ents,compr ise sever al elements. Central to these syst emsare one or more osci llator circuits that gen erate therudim ents, in period and phase, of the expres sedmotor activ ity. Exc itatory inputs from higher cente rs,from sensor y input, or from within the circuit s them-selves stimulate CPG outp ut to pass from a ‘resting’stable state, that is, without oscillatio ns, to one that isunstabl e and hen ce oscilla tes with a freque ncy thatmay or may not mat ch that obs erved in the intactanima l. Most CPG s are form ed entirely, or ne arlyso, of inte rneurons . How ever, motor neurons mayconstitut e most of the CPG, a s in the stomatoga stricsystem of crust acea; they may be weak ly invol ved inpattern g eneration, as in the leech swim CPG ; or theymay merely serve as follow ers to drive musc le con-tracti ons, a s in the lamprey swim circuits. Sensoryfeedback arises from stretch receptors in muscles, pro-prioceptors, sensory hairs as in crustacean swimmerets,cuticle receptors that signal load in insects, and stretchreceptors in the CNS itself, as in lamprey. These recep-tors may be spiking or nonspiking, but their function isto provide position, load, velocity, and angle informa-tion to the CPG – afferent information that informs theCPG whether the movement commanded is appropri-ately executed. Alternatively, sensory input modifiesCPG function more drastically, as during animal walk-ing, in which sensory processes control phase relation-ships among limbs and the intensity of motor neuronoutput and may advance, retard, initiate, or preventph as e t ra ns it ion s.

Experimental Approaches: Techniquesand Animal Preparations

Expe riment s to deter mine the nature of the sensor yrecep tors an d their role in CPG modul ation have


encompassed a wide range of animal preparationsand experimental approaches.

Experimental Approaches and Techniques

Comparison of CPG output and movements of intactanimals One methodology employed nearly univer-sally to assess the relative importance of CPG circuitsand sensory feedback in the control of animal move-ments is to compare the neuronal activity patternsexpressed in reduced preparations with those ofintact, behaving animals. Such comparisons revealfour major aspects of rhythmic activity that are modi-fied by sensory feedback: cycle period, activity ampli-tude, phase relationships among local outputs, andintersegmental phase relationship. There is a widerange in the relative strength of sensory feedbackeffects, as illustrated in Figure 2, which shows thatcycle periods of fictive (isolated CNS) swimmingactivity in both leech and lamprey are significantlygreater than in the intact animal. However, phaserelationships remain unchanged by removal of theperiphery in the lamprey whereas intersegmentalphase lags are reduced by nearly 50% when sensoryfeedback is eliminated in leeches.

Sensory entrainment A secondwidely used techniquefor determining the nature and strength of sensory feed-back is to perform entrainment experiments. With thisapproach, either the body itself (in semi-intact prepara-tions) or sensory receptormembrane potential is modu-lated rhythmically by the experimenter while the CPG

In vitro

DP(4)

DP(4)

DP(10)d

P

R

R

R

RDP(10)

Intact

1 sa b

1 s

Figure 2 Activity patterns during swimming locomotion: patterns ge

animals. (a) Leech swimming. The upper traces (in vitro) were obtaine

cord with electrodes attached to the dorsal posterior (DP) nerves of s

electrodes implanted onto the DP nerves of segments 4 and 10 during

axon impulses of cell DE-3, a motor neuron that innervates dorsal long

delay. (b) Lamprey swimming. The upper traces (in vitro) depict ventral

electromyograph records obtained from an intact swimming lamprey.

side at the segments indicated. Fictive swimming was elicited by bat

calibrations. (a) Reproduced from Pearce RA and Friesen WO (198

of in situ and isolated nerve cord activity with body wall movement

(b) Reprinted from Wallen P and Williams TL (1984) Fictive locomotion

intact and spinal animal. Journal of Physiology 347: 225–239, with pe

is generating rhythmic output. For many systems,movements or direct current injection into sensoryneurons can force the CPG to generate cycle periodsthat are up to �50% of the unperturbed values.Figure 3 illustrates the entrainment technique as it isapplied to the swimming rhythm in lamprey. Herephysical movements of the rostral or caudal ends ofa spinal cord/notochord preparation entrain the CPGsas the movement frequency is set to values both belowand above those detected when movements areabsent. Such experiments demonstrate that sensorystructures, in this case edge cells, have access to theCPG and can modify its properties. Related, alterna-tive approaches are to impede limb or body move-ments; place a limb into a particular, fixed position;or assess the effects of brief current injection intosensory neurons. Like the entrainment procedure,these alternative methods provide useful informationabout both the nature and the strength of sensoryinput in the expression of rhythmic movements.

Animal Preparations

Six preparations and behaviors are described here toillustrate current procedures of, and results from,studies on the relationships between CPG-generatedrhythms and sensory inputs during the expression ofrhythmic movements. These behaviors are flying inlocusts, swimming in leeches and lamprey, swimmeretbeating in crayfish, and walking in stick insects andcrustacea.

In vitro

R 6

27

47

R 6

23

46

Intact

1 s

0.3 s

nerated by CPGs compared with those expressed by nearly intact

d from a preparation consisting of the isolated leech ventral nerve

egments 4 and 10. The lower traces (intact) were obtained from

swimming in a nearly intact leech. The bursts in these records are

itudinal muscles. P is the cycle period, and d is the intersegmental

root activity during fictive swimming. The lower traces (intact) show

Letters R and numerals indicate that recordings are from the right

h application of 0.5mmol l�1 D-glutamate. Note the different time

4) Intersegmental coordination of leech swimming: Comparison

. Brain Research 299: 363–366, with permission from Elsevier.

in the lamprey spinal cord in vitro compared with swimming in the

rmission from Blackwell Publishing.

Experimental setup

a

b

c

1 2 3

4

4 5Right

Resetting

Motormovement

T 0 = Average resting cycle time (cycles 1–4)

T 1 = Perturbed cycle time (cycle 5)

d /T 0 = Stimulus phase (0 to 1.0)

d /T = Movement phase (0 to 1.0)

Entrainment

d = Delay

d = DelayT = Burst cycle time

T m = Movement cycle time

BD = Burst duration

Left

Right

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6 7

T0

d

T

T md

T1

Right

Left

RT.

LT.

Motor

BD

RT.

LT.

Figure 3 Schematic diagram for entrainment experiments in lamprey. (a) Diagram of the in vitro notochord/spinal cord preparation. The

caudal (right (RT.)) end of the preparation was rhythmically deflected with a pen motor while the preparation was immobilized to the left

(LT.) of the arrowheads. (b) Step inputs. Brief movements (300 ms) of the caudal end at selected phases in the swim cycle were used to

determine phase changes (as a fraction of the cycle period) to generate phase response curves (not shown). (c) Entrainment methodol-

ogy. Sinusoidal movements with a range of cycle periods (T ) were applied to the preparation; cycle period and the phase relationship (d/

T ) between the imposed signal and the fictive motor output were measured. Reprinted from McClellan AD and Jang W (1993) Mechano-

sensory inputs to the central pattern generators for locomotion in the lamprey spinal cord: Resetting, entrainment, and computer

modeling. Journal of Neurophysiology 70: 2442–2454; used with permission.


Locust flight Locust flight was the first behavior forwhich the central role of a CPG was widely accepted.Ironically, locust flight is also among the first clearexamples of sensory feedback coordinating animalmovements in a well-defined system. Comparisonsof flying in nearly intact but tethered animals withthe output of the flight CPG in the absence of sen-sory input reveal the following differences. Wingbeat

frequency in tethered flying locust is approximately15–20Hz, whereas deafferented preparations exhibitfrequencies about half of those values. Moreover,nearly intact tethered locusts stimulated with air cur-rents in a wind tunnel fly continuously, whereasreduced preparations lacking sensory feedback soonterminate the CPG-generated pattern. Stimulation offorewing stretch receptors alters the expressed

Wingelevation

566/7 D

Dep

Wingdepression

TegulaeStretch

receptors

EINs

d

Elev

DINs

Figure 4 Diagram illustrating identified interactions between sen-

sory afferents and the locust flight central pattern generator (CPG).

EIN, elevator interneurons; DIN, depressor interneurons; 566 iden-

tified interneurons that participate in the generation of the flight

rhythm only when they receive phasic input from tegulae during

flight. Elev, elevator motor neurons; Dep, depressor motor neurons;

d, delayed excitation; D, long delay, with input arriving at the depres-

sor neurons one cycle subsequent to one that generated the sen-

sory signal. With permission from Pearson KG and Ramirez J-M

(1997) Sensory modulation of pattern-generating circuits. In:

Stein PSG, Griller S, Selverston AI, and Stuart DG (eds.) Neurons,

Networks, and Motor Behavior, pp. 225–235. Cambridge, MA: The

MIT Press.ã 1997 Massachusetts Institute of Technology.


rhythm in several ways. First, repeated stimulationphase-locked to the flight pattern increases wingbeatfrequency. Second, such stimulation prolongs theexpression of the motor pattern. These effects arephase-dependent, indicating that they function on acycle-by-cycle basis rather than through general exci-tation. Third, stimulation of both forewing stretchreceptors at frequencies near the wingbeat frequencyentrains the flight rhythm, provided that the fre-quency of the entraining signal is within 20% of thenatural frequency. Single stimuli applied to the stretchreceptors can, if appropriately timed, reset the phaseof the flight rhythm. The rhythm can also be entrainedby sinusoidal depression and elevation of a forewingwhile the locust is flying in a wind tunnel. The entrain-ment range for this more natural stimulation is some-what smaller, with stable entrainment only when theentraining frequency is within 15% of control.More than modifying the CPG rhythm, forewing

stretch receptors appear to be important componentsof the flight oscillator in locusts. Intracellular record-ings from flight CPG interneurons reveal short-latencyexcitatory input from forewing stretch receptors.Because these receptors are phasically active duringflight, can entrain and reset the flight rhythm, andappear to have monosynaptic inputs to CPG interneur-ons, they are considered to be important elements in thesystem generating the normal flight rhythm duringwing elevation (Figure 4). Effects of these receptorsand of the tegulae also increase the precision of coordi-nation among the wings. The conclusion is that theforewing stretch receptors and the tegulae (activatedby wing depression) are peripheral elements of a com-plex oscillator system that comprises the CPG andperipheral sensory feedback loops.

Leech swimming Medicinal leeches are elongated,segmental worms 5–15 cm in length when fullyextended. During the prologue to swimming, theleech body flattens and extends in length and width,providing a nearly uniform, flattened profile that isefficient for swimming locomotion. Leeches swim bywhole-body undulations that are seen in side-view asa traveling rostrocaudal sinusoidal wave with a cycleperiod range of 0.3–1 s. The most efficient waveformfor this whole-body mode of swimming is a quasi-sinusoidal body wave comprising one wavelength.Commensurate with this theoretical expectation, atany instant, about a single wave length is expressed byswimming leeches. The rhythmic movements of thebody are generated by locally antiphasic shortening–lengthening cycles in dorsal and ventral longitudinalmuscles. These contraction rhythms, which act againstthe elevated internal body pressure generated by activ-ity of the flattener muscles, exhibit rostrocaudal phase

delays and thereby generate the observed travelingbody wave. With some 18–20 body segments activelyparticipating in generating the swim undulations, theintersegmental phase lags in swimming animals areabout 20� per segment.

Like other rhythmic movements, the activity cycles,cycle period, and intersegmental phase lags expressedby swimming leeches find a rudimentary origin in aset of interneurons that constitute the CPG. The unitelements of the CPG are found in each midbodyganglion of the leech ventral cord. Although singleganglia are capable of brief, weak swim oscillationswhen exposed to 50mmol l�1 serotonin, at least twosegments are required to generate strong oscillationsand intersegmental phase delays. The leech swimCPG comprises more than 13 interneurons per seg-ment, with some participation by sets of dorsal andventral inhibitory motor neurons. The central oscilla-tor network does not, however, generate the full

DSR

DE

DI

VI

VE

28

208

115

IN MN

DLM

VLM

33

VSR

Figure 5 Interactions between stretch receptors and swim-

related neurons in leeches. Only a subset of central pattern gener-

ator (CPG) neurons (cells 115, 208, 28, and 33) and the phasically

active motor neurons are depicted. The ventral stretch receptor

(VSR) conveys tension information from the ventral longitudinal

muscle (VLM) directly to at least one CPG interneuron, cell 33.

IN, interneurons. Motor neuron (MN) designations: DE, dorsal

excitor; DI, dorsal inhibitor; VI, ventral inhibitor; VE, ventral excitor;

interaction symbols: filled circle, chemical inhibition; ‘T,’ excitation;

resistor, nonrectifying electrical interaction. Dashed interactions

appear to be indirect. Interactions between the DSR and the

CPG remain unexplored. Reprinted from Cang J, Yu X, and

FriesenWO (2001) Sensorymodification of leech swimming: Inter-

actions between ventral stretch receptors and swim-related neu-

rons. Journal of Comparative Physiology 187: 569–579,

figure 1(b), ã 2001 Springer-Verlag, publisher. With kind permis-

sion of Springer Science and Business Media.


rhythm exp ressed in the inta ct animal. The cycleperio d gen erated by the CPG ranges from 0.6 to 2 s,barely overlap ping the perio d range observe d inintact animal (0.3–1 s), and interse gmental phaselags expres sed by the CPG (about 10o per segm ent)are only 50% of these of intact anim als ( Figure 2(a) ).Thus the isolated CPG does not pro duce neuronalactivi ty patterns for fast, efficient locom otion.The sensor y inputs that, together with CPG cir-

cuits, genera te neuron al activity pa tterns ap propriatefor efficient swim min g arise, at least in part, fromsegmen tal stretch rece ptors, whose somata a re asso-ciated with dorsal an d ventral longitudi nal muscles.Stretchi ng the lee ch body wall indu ces a hyperpol ari-zation in these recep tors, which have peri pherallylocated somat a and dend rites an d whose giantaxon s conduct this signal to the CNS electron ically.The importanc e of sensor y mechanis ms in leech

swim ming locom otion was recognize d from thebeginni ng of systema tic studies of this behavi or. Forexampl e, lee ches were foun d to swim at a lowerfreque ncy in high viscosi ty media. Mo reover, leecheswhose movem ent was restricte d mec hanica lly so thatthey were unab le to execut e the nor mal swim undu-lation alt ered their movement s or ab orted ongoingtraveli ng wave s. More rece ntly, sever al types ofexperi ments de monstrat ed that the stretch receptorscan modify the basic activi ty pa tterns gen erated bythe CPG. First, in nerve cord–body wall prepara tions,these rece ptors encode musc le tension informat ionvia mem brane potential osci llations, wi th ampl itudesup to 10 mV recor ded as the axons enter the ganglia.Second, rhythm ic curren t injection into these recep-tors can alter inte rsegment al phase lags by �5 � in aphase- dependent manner. Thi rd, experime ntallyinduce d stretch recep tor mem brane potent ial oscilla-tions entra in the CPG rhythm if the imp osed rhythmis withi n about 50% of the free-runni ng CPG rhythm .Fourth, brie f (sev eral second s long) current pulse sinject ed into a stretch rece ptor shift the phase of theventr al nerve cord swim osci llations. Finally, there isdirect ele ctrical coupling between a t least one of thestretch rece ptors an d a CPG inte rneuron ( Figure 5).Henc e, as for locus t flight , the cir cuits that generatethe swim ming rhythm in the leech compr ise boththe CPG a nd the peri pheral stre tch.

Lamprey swim ming La mpreys are primit ive fishthat swim via anguillifor m (eellike) undulat ions,that, as in leeches, compr ise about one wavele ngthat any moment. The traveling wave results from anti-phasic contraction of segmental muscles and fromrostra-caudal delays of 1% of the cycle period persegment for a 100-segment animal. Intact lampreysswim with cycle periods ranging from about 0.13 s to

more than 0.6 s. The spinal cord of lampreys includes aseries of local CPGs. Comparisons of swimming move-ments in intact animals and motor neuron activitypatterns generated within the stationary spinal cord(fictive swimming) show similar patterns (Figure 2(b)).Although the range of cycle perio ds obtained by alter-ing the con centratio n of the swim -inducing excitat oryamino acids (0.7– 2 s) in fictive swim ming overl apsthat observe d in the intact animal, the CPG -generate dperio d is normall y ab out tw ice that of the intact ani-mal. Unl ike results from lee ches, the interse gmentalphase lags in lamp reys do not differ marke dly inisolate d prep arations compar ed with those of intactanima ls (Figure 2(b)). Thus sensor y feedba ck appearsto be essen tial for setting the cycle period but notfor phase con trol during undi sturbed swim ming inthe lamprey.

Sensory feedba ck during the side -to-sid e undula-tions of the swim ming lamprey arises, in part, fromsegmen tal ‘edge cel ls’ withi n the spinal cord. Thesecells make synaptic contacts with CPG neurons andwith motor ne urons. Inte ractions between the CPGand the ed ge receptors in the intact animal may, likethe CPG itself, compr ise a funct ional osci llator.Experi ments on sp inal cord–not ochord pr eparationsdemons trated that the CPG rhythm can be entrained

Basalganglia

Forebrain

Brainstem

Spinalcord

Sensory

SR-E

SR-I

Sensory

Excitatory, glutamate

Inhibitory, glycine

SR-E

SR-I

E E

M ML L

I I

Vision

Olfaction OlfactionVTH

MLR MLR

Trigem. Trigem.RS RS

VTH

Vision

Figure 6 Circuits underlying swimming movements in lam-

preys. A population of reticulospinal neurons (RS) excites the

spinal interneurons and motor neurons. Excitatory interneurons

(E), in turn, excite other spinal neurons, including inhibitory inter-

neurons (I) that cross the midline to inhibit neurons on the contra-

lateral side, and lateral interneurons (L) that inhibit ipsilateral

interneurons and the motor neurons (M). Spinal stretch receptor

neurons (edge cells) include two types; excitatory neurons (SR-E)

that excite ipsilateral neurons and inhibitory neurons (SR-I) that

inhibit contralateral neurons. Symbols denote populations of cells,

not single neurons. Additional control of this systemappears to arise

from the ventral thalamus (VTH), the trigeminal nuclei (Trigem.), and

themesencephalic locomotor region (MLR). Reproduced fromGrill-

ner S andWallen P (2002) Cellular bases of a vertebrate locomotor

system: Steering, intersegmental and segmental co-ordination

and sensory control. Brain Research Reviews 40: 92–106, with

permission from Elsevier.


by mechanical movement of either the rostral or thecaudal ends. That is, sensory input arising from thesemovements could alter the 0.7Hz ‘natural’ frequencyby a maximum of 50% above and no more than 25%below this control frequency. The range of entrain-ment depended on the length of the preparation.Short preparations (25 segments) yielded an entrain-ment range that was nearly twice the range for longerpreparations (50 segments). Relative entrainment wasalso observed with input-to-expressed frequencyratios of 1:2 and 2:1.Brief movement pulses applied to the spinal cord,

as well as current injection into edge cells, can resetthe phase of the swimming rhythm of lampreys.Movement pulses, used to generate phase responsecurves for the spinal cord–notochord preparations,showed phase advances during two-thirds of thecycle, with the largest phase shifts near mid-cycle.Again, it seems likely that, as for locusts and leeches,normal locomotion in lamprey arises both fromsegmental CPGs and from sensory feedback circuits(Figure 6).

Crustacean swimmeret beating Crayfish, lobsters,and other decapod crustaceans have abdominalappendages, swimmerets, that beat with metachronalrhythms. The paired segmental CPGs in this system,unlike those described above, provide a basic rhythmthat is nearly identical in both cycle period and inter-segmental phase lag, about a quarter of the cycleperiod, to those observed in the intact animal.Although the need for sensory feedback in undis-turbed beating is not obvious, execution of swimmeretmovements is nonetheless monitored via a set of sen-sory receptors, including proprioceptors that providephasic feedback.When, for example, themovement ofa swimmeret is experimentally impeded, by fixing thelimb at either the retracted or protracted phase in itsmovement cycle, the central rhythm sometimes stops,sometimes decelerates. In addition to the propriocep-tors, lobsters have hairs whose deflection in responseto water movements engendered by swimmeret beat-ing can provide rhythmic afferent information. Also,there are two types of hypodermal mechanoreceptorsthat are likely to be activated when swimmerets beatrhythmically. It appears that swimmeret mechano-receptor activity, although not required for generatingan appropriate activity pattern for swimmeret move-ment, contributes to the movement of these appen-dages when normal movement is somehow impeded.

Insect and crayfish walking The neuronal activitypatterns that underlie animal walking movements areconsiderably more complex than the neuronal patternsthat underlie flying, swimming, or swimmeret beating.

Most animals that utilize walking locomotion havemultiple limbs, with each limb comprising multiplesegments. Added to those factors is the daunting taskof generating effective limb placement on a highlyunpredictable substrate. It is therefore not surprisingthat sensory receptors are closely tied to CPG elementsassociated with this form of locomotion.

Many forms of animal locomotion can be viewedas the rhythmic alteration of two phases, a powerstroke, in which the animal exerts forces on its envi-ronment that propel it forward, and a return strokethat returns the limb to the original position forthe next power stroke. A major focus for studies ofsensory input to the CPG circuits that underlie thewalking cycle is the control of transitions betweentwo phases in walking locomotion, the stance and


the swing phases. Two additional foci are the controlof intra- and interjoint phase angles.One of the best-studied walking behaviors is

that of the stick insect. Each leg in the stick insecthas three main joints that are responsible for move-ments in the horizontal and vertical planes. Musclesassociated with the thoracocoxal (TC-) joint drive theleg back and forth, whereas the coxatrochanteral(CTr-) and femur–tibia (FTi-) joints (Figure 7(a))are involved in placing the tarsal segment firmlyonto the substrate (during the stance phase) or raisingit into the air (during the swing phase). With appro-priate stimulation, deafferented thoracic ganglia canbe induced to generate the antagonistic motor neuronactivity patterns that cause rhythmic joint movements.Because there is little or no coordination among

Tc-joint

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–

–

Lev Lev

Lev

Dep

Figure 7 Schematic of sensory influences on the movements of

the middle leg of the stick insect. (a) Cartoon of the stick insect leg

showing the three main leg joints. (b) Extension position signals

(ext. signals) from the FTi-joint switch the phase of the central

pattern generator (CPG; Lev to Dep) in the adjacent joint (CTr-

joint). The CPGs are denoted by boxes with two interacting neu-

rons, with the active phase indicated by a filled circle. Arrows

indicate interactions, but not specific synapses, between hypothe-

sized CPG elements and the antagonistic sets of motor neurons

(MNs; rectangles; filled elements are active) they control. (c) Load

signals (load increase (incr.)) from the CTr-joint switch the state

of the TC-joint CPG (Pro to Ret). TC-joint, –thoracocoxal joint;

CTr-joint, –coxatrochanteral joint; FTi-joint, femur–tibia joint; Ret,

retraction/retractor; Pro, protraction/protractor; Dep, depression/

depressor; Lev, levation/levator; Flx, flexion/flexor; Ext, extension/

extensor. Reprinted from Buschges A (2005) Sensory control and

organization of neural networks mediating coordination of multi-

segmental organs for locomotion. Journal of Neurophysiology 93:

1127–1135, used with permission.

groups of motor neurons associated with differentjoints in such a preparation, it appears that a unitCPG drives muscles at each joint. The specific neuro-nal circuits constituting these CPGs remain largelyunidentified; however, it is clear that activity inthese CPGs is closely coordinated by sensory signalsarising from leg proprioceptors and cuticular strainreceptors. Coordination of the movements of individ-ual joints occurs by a cascade of sensory informa-tion whereby signals from one joint in a leg reset thephase of the CPG that drives a second joint in that leg.These signals include two temporally related sensorymodalities: leg weight load and joint position. Theeffects of such sensory signals are weighted within theCNS to generate locomotory movements.

The specific roles of sensory influences on the CPGsthat control the main joints in the stick insect are nowknown for the phase transitions that occur duringstep cycles. Two such transitions are illustrated inFigures 7(b) and 7(c). In Figures 7(b), movement-induced signals from FTi-joint receptors (extensionsignals, lower left) cause a transition from swing tostance phase. This occurs because this sensory inputswitches the CPG of the CTr-joint leg to the depressorphase, activating the depressor motor neuron, therebylowering the leg to begin the stance phase. Next, inFigure 7(c), load receptor activation in the CTr-joint(load increase, left) induced by initiation of the stancephase forces a phase transition from protraction toretraction onto the TC-joint CPG, thereby activatingretractor motor neurons that act at the TC-joint andbegin the forward propulsion phase of the leg stepcycle. Sensory receptor input often has two effects,such as when an increased load increases the activityin flexor motor neurons and hence to muscles thatsupport the animal’s weight while simultaneouslyinhibiting the antagonistic extensors. There appearto be two general coordinating systems: one that initi-ates transitions between phases of the walking cycle,and one that determines its direction. Computer simu-lations have demonstrated that the known sensoryinputs to control limb motions can, when implemen-ted in a simulated neuronal controller, generate legstepping movements. Here again, rhythmic locomo-tory movements arise from combined CPG and sen-sory interactions. For the stick insect, the role ofsensory input influences not only period and phasebut the very transitions of the CPG between phasesof the activity cycle.

As in stick insects, walking locomotion in thecrayfish also arises from CPGs strongly influencedby sensory input. However, unlike the nearly inde-pendent joint CPGs of the stick insect, walkingCPGs express a coordinated walking rhythm in deaf-ferented preparations. That is, the crayfish CPGs


include effective interactions within the CNS whilestill requiring sensory input to ensure appropriatecycle periods and stable phase relationships. Althoughthe CPGs associated with the eight walking legs incrayfish remain unidentified, at least one sensorystructure, the thoracocoxal muscle receptor organ(TCMRO), is known to interact with the CPGs.Rhythmic stretching and releasing of the TCMROcan entrain the CPG, not only locally, but acrossother legs. The data show that the interactionsbetween sensory input and the CPGs are strong, forthe phase relationship between an imposed stimulusrhythm, and the entrained walking cycles is nearlyconstant. The suggestion is that the walking rhythmis not entrained but actually driven by sensory input.Relative coordination also occurs, with stimulus–response periods of 2:1 or 1:2 when the stimulusfrequency lies outside the entrainment range. Directcurrent injection into the TCMRO afferents alsowas effective. Overall, sensory input, as in the stickinsect, appears to trigger transitions between phasesof the movement cycle, and hence sensory input pro-vides essential information to the locomotory CPGin crayfish.

Conclusion: Beyond Sensory Modulation

Just as motor neurons sometimes are integral membersofCPGs, even if they are not strictly limited to theCNS,so sensory neurons and muscles may be essential com-ponents of circuits that generate rhythmic movements.Sensory input varies in importance among the highlydiverse circuits that generate wingmovements in locustflight, swimming undulations in the medicinal leechand lampreys, and swimmeret beating and walkinglocomotion in insects and crayfish. For understandingthe physiological bases of rhythmic movements, itappears to be unhelpful to construct artificial divisionsbetween CPGs, motor neurons, muscles, and sensoryfeedback. Amore useful approach is to identify oscilla-tory subcircuits wherever they occur, whether withinthe CNS or not; and whether comprising interneurons,motor neurons, effector structures, or sensory recep-tors. Such subcircuits, together with their mutual inter-connections, generate the highly variable and adaptiveoscillating patterns that underlie rhythmic animalmovement.

See also: Behavioral Hierarchies; Central Pattern

Generators; Command Systems; Hormones and

Behavior; Neuromodulation; Pattern Generation; Swim

Oscillator Networks; Swimming: Neural Mechanisms ;

Walking in Invertebrates.

Further Reading

Buschges A (2005) Sensory control and organization of neural net-works mediating coordination of multisegmental organs for

locomotion. Journal of Neurophysiology 93: 1127–1135.

Cang J, Yu X, and Friesen WO (2001) Sensory modification ofleech swimming: Interactions between ventral stretch receptors

and swim-related neurons. Journal of Comparative Physiology187: 569–579.

Delcomyn F (1980) Neural basis of rhythmic behavior in animals.Science 210: 492–498.

Elson RC, Sillar KT, and Bush BMH (1992) Identified pro-

prioceptive afferents and motor rhythm entrainment in the

crayfish walking system. Journal of Neurophysiology 67:530–546.

Friesen WO and Cang J (2001) Sensory and central mechanisms

control intersegmental coordination. Current Opinion inNeurobiology 11: 678–683.

Grillner S and Wallen P (2002) Cellular bases of a vertebrate

locomotor system: Steering, intersegmental, and segmental

co-ordination and sensory control. Brain Research Reviews40: 92–106.

Hooper SL and DiCaprio RA (2004) Crustacean motor pattern

generator networks. Neurosignals 13: 50–69.Kristan WB Jr, Calabrese RL, and Friesen WO (2005) Neuronal

control of leech behavior. Progress in Neurobiology 76:

279–327.

McClellan AD and Jang W (1993) Mechanosensory inputs to the

central pattern generators for locomotion in the lamprey spinalcord: Resetting, entrainment, and computer modeling. Journalof Neurophysiology 70: 2442–2454.

Pearce RA and Friesen WO (1984) Intersegmental coordinationof leech swimming: Comparison of in situ and isolated nerve

cord activity with body wall movement. Brain Research 299:

363–366.

Pearson KG and Ramirez J-M (1997) Sensory modulation ofpattern-generating circuits. In: Stein PSG, Griller S, Selverston AI,

and Stuart DG (eds.)Neurons, Networks, and Motor Behavior,pp. 225–235. Cambridge,MA:MITPress.

Rossignol S, Dubuc R, and Gossard J-P (2006) Dynamic sensori-motor interactions in locomotion. Physiological Reviews 86:

89–154.

Sherrington CS (1947) The Integrative Action of the NervousSystem, 2nd edn. New Haven, CT: Yale University Press.

Wallen P and Williams TL (1984) Fictive locomotion in the lam-

prey spinal cord in vitro compared with swimming in the intact

and spinal animal. Journal of Physiology 347: 225–239.Wilson DM (1961) The central nervous control of flight in a locust.

Journal of Experimental Biology 38: 471–490.

Yu X and Friesen WO (2004) Entrainment of leech swimming

activity by the ventral stretch receptor. Journal of ComparativePhysiology 190: 939–949.

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Encyclopedia of Neuroscience || Central Pattern Generators: Sensory Feedback