Postural Control Man: Thedownloads.hindawi.com/journals/np/2005/637472.pdf · · 2014-05-08NEURALPLASTICITY VOLUME12, NO.2-3,2005 PosturalControlin Man:ThePhylogeneticPerspective

NEURAL PLASTICITY VOLUME 12, NO. 2-3, 2005

Postural Control in Man: The Phylogenetic Perspective

Albert Gramsbergen

University ofGroningen, Medical Physiology, 9713 A V Groningen, the Netherlands

ABSTRACT

Erect posture in man is a recent affordancefrom an evolutionary perspective. About eightmillion years ago, the stock from which modernhumans derived split off from the ape family,and from around sixty-thousand years ago,modern man developed. Upright gait andmanipulations while standing pose intricatecybernetic problems for postural control. Thetrunk, having an older evolutionary history thanthe extremities, is innervated by mediallydescending motor systems and extremity musclesby the more recent, laterally descending systems.Movements obviously require concerted actionsfrom both systems. Research in rats hasdemonstrated the interdependencies betweenpostural control and the development of fluentwalking. Only 15 days after birth, adult-likefluent locomotion emerges and is criticallydependent upon postural development. Vest-tibular deprivation induces a retardation in

postural development and, consequently, aretarded development of adult-like locomotion.The cerebellum obviously has an important rolein mutual adjustments in postural control andextremity movements, or, in coupling the phyio-genetic older and newer structures. In thehuman, the cerebellum develops partly afterbirth and therefore is vulnerable to adverseperinatal influences. Such vulnerability seems to

Reprint requests to: Albert Gramsbergen, University ofGroningen, Medical Physiology, 9713 AV Groningen, TheNetherlands; e-mail: [email protected]

(C) 2005 Freund & Pettman, U.K.

justify focusing our scientific research effortsonto the development of this structure.

INTRODUCTION

"Posture" might be defined as the position ofthe body in relation to the gravitational vector andof the body-segments in relation to each other,both in static and in dynamical conditions (e.g.,Gramsbergen, 1998). Deficient postural control inhuman infants is considered an important factor inseveral developmental disorders concerning motorcontrol (Aicardi & Bax 1992), and for that reason,this aspect has been in the center of interests ofrehabilitation therapists, pediatric neurologists andneurobiologists, for example. When consideringpostural control from a neurophysiological pointof view, it is important to realize that this controlas such is an abstraction from motor control.Indeed, abnormalities in motor patterns might betraced back to abnormalities in controlling thetrunk or to abnormalities in maintaining equili-brium. Therefore, assessing the reactions toperturbations or analyzing such motor patterns as

reaching in babies or’ rearing in rats can help toinvestigate this specific aspect of motor control.Yet, movements and postural control in normallyfunctioning individuals are fully integrated anddistinguishing one or the other aspect in an

ongoing movement basically is impossible. On theother hand, it should be realized that the trunk andneck, instrumental in keeping the body erect or

straight, and the extremities involved in locomotorand manipulative movements have different phylo-genetic histories. The trunk has a history stretching

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78 ALBERT GRAMSBERGEN

over billions of years, whereas the extremities arefrom a more recent past, and the fine and delicateneural control of finger move-ments emerged onlya few million years ago. Interestingly, thesedifferential ancestries are reflected in importantdifferences in those sub-systems of the centralnervous system that govern the trunk andextremity muscles, respectively. A similar exampleis the visual system in man, in which the fovea,projecting via the geniculate nucleus to the visualcortex, is fully integrated with the subcorticalretino-tectal system active in directing gaze(Deacon, 1992). The latter system (involvingperipheral retinal fields, tecto-spinal, and tecto-bulbar projections) developed early in evo-lution,whereas acuity and color vision (depending upontightly packed cones in the fovea and on corticalcircuitry) has developed only recently. Theseexamples illustrate that phylogenetically oldersystems can persist alongside newer systems, bothbeing fully integrated into one functioning system.Yet, differences between older and newer elementscan remain apparent, generally by their circuitriesand localization, often by their develop-mentalpathways and sometimes by differential vulner-abilities to trauma. This is the background forconsidering in this essay some evolutionaryaspects of postural control and movements.

EVOLUTION OF TRUNK AND EXTREMITIES

Evolution is based upon the selection of thosevariations in the genome that provide groups ofindividuals with increased adaptational possibilities(Gould, 2000). Evolution principally is an autono-mous process, new behaviors became possible andnew structures spontaneously emerged during evo-lution rather than being caused by it (Dover,2000).The possibilities to make use of alternativeand richer food supplies, particularly in circum-stances of diminishing resources, have given certain

varieties decisive advantages over others whocould not, and the need for food in particular hasbeen considered a powerful selective agentthroughout evolution. The evolution from ancientforms of animal life clearly illustrates this point.The earliest animals reside in the water, remainingon one place, and wait for food to come to them.Sea anemones with a nervous system consisting ofa diffuse network of neural cells are examples ofsuch ’primitive’ creatures. Sea anemones do moveby changes of posture, they even present moods bypostural changes (Reisinger, 1926) and survive bydigesting the food passing by. More advanced arefishes, belonging to an early order of vertebrates.Fishes are able to move towards their foodsources. Swimming in fish is effected byundulating movements of the trunk, mostly in aside-to-side fashion. Their side-fins are not trueextremities but rather serve to stabilize the bodyduring swimming.

Amphibiae, more advanced vertebrates, arefurnished with extremities that enable them tomove effectively on firm ground from one pond tothe next, allowing them to find fresh water orricher food sources. Amphibiae developed lungs,which obviously are an essential requirement toremain in terrestrial conditions for extendedperiods. The extremities, particularly the musclescounteracting gravity, serve to keep the belly freefrom the ground (Romer, 1969), but progression inamphibiae, as in fish, is mainly effected byundulatory movements of the trunk.

In reptiles, the extremities are more powerfuland in some varieties provide animals with a fairdegree of agility (obviously, snakes are in thisrespect an exception among reptiles). Interestingly,the thecodonts (to a certain degree resemblingcrocodiles) living around 240 million years ago inthe triassic period, tended towards bipedal loco-motion (Chatterjee, 1982). Other species of thethecodontiae obviously were able to fly. Somevarieties lived in trees, others must have climbedtrees and glided back to the ground, and still other

POSTURAL CONTROL IN MAN, THE PHYLOGENETIC PERSPECTIVE 79

forms actively flew. Obviously, these thecodontswere transitional forms between reptiles and birds.

At a later stage in evolution, mammalsdiverted from the reptiles, giving birth to life-stock. Their strong and long extremities allowquadrupedal mammals to move swiftly andefficiently. Cats, dogs, horses, for example, areable to walk slowly but also to trot or gallop andjump, all depending on subtle adjustments in inter-and intra-limb coordination (Grillner, 1981). Theextremity movements in mammals have taken theprimacy in propulsion, whereas the control of thetrunk subserves keeping the trunk and the headstabilized in space. Hominids are specificallydistinguished from monkeys and apes by theirbipedal gait. The body is lightly built; the legs arelong and strong, the arms being relatively short.Whether the need for food or a change in the diethas been the selective agent in the evolution fromquadrupedal to bipedal gait and other develop-ments is not clear. Their evolution is indicated byan increase in brain size, by the ability tocommunicate effectively, by increasingly efficientways to walk swiftly over long distances, and bytheir manual skills, enabling them to build and usefine tools, to mention only a few aspects. Theseaffordances have tremendously increased the poss-ibility to exploit resources efficiently, to integrateinto social communities, to share new knowledgeand by that, to solve common problems. Theseaspects decisively have given them advantagesover their more primitive predecessors.

Based on biochemical extrapolations, it isestimated that only between eight and five millionyears ago, the first hominids, the australopithe-cines, split off from the ape family (White et al.,1994; Leakey et al., 1995; Ward et al., 2001). D.C.Johanson in Mary Leaky’s team in 1978 inTanzania discovered the footprints of threeaustralopithecus individuals in volcanic ash, whichsolidified after they had crossed it. Estimatesbased on skeletal remains of these homoaustralopithecus afarensis indicated that they were

to 1.5 meters tall, weighed about 50 kilograms,with a brain size of 400 to 500 mL, which is aboutone third of that in modern humans. Footprints, aswell as the shape of the hips, knees, and femur,indicate that such individuals walked bipedally(Martin, 2002). The toes being closely togetherand the big toes not being opposed to the othertoes resemble the foot and the position of the toesin modern man. Based on artifacts that were foundin the area, such individuals apparently were ableto produce tools.

About 2.4 million years ago, new types ofhominids appeared in eastern and southern Africa,with a more advanced and distinctly ’human’build, the homo habilis, the handy men, to 1.5meters tall and with a brain size of between 500and 800 mL. From 1.8 million years ago, a newvariety developed in Africa, the homo erectus,being 1.3 to 1.5 meters tall and distinguished fromthe earlier homo habilis by an increased brain sizeof 800 to 1200 mL. Hominids with thesecharacteristics obviously migrated from onemillion years ago to Asia, the Indonesion isles, andpossibly to Europe as well (Stringer, 2002). Basedon artifacts that were found in Georgia, it appearedthat they used tools made of wood, which must

have required rather sophisticated fabricationtechniques or, advanced manipulative skills. Homosapiens, the variety to which modern humansbelong, emerged about four hundred thousandyears ago. These hominids had a larger brain and askull that approached the modem form. A well-known specimen is the homo neanderthalensis,and similar skeletons have been found elsewherein Germany, in Wales, in England, and in France.They lived until 30,000 years ago, had brain sizesranging between 1200 and 1750 mL, weighed 65kilograms, and were up to 1.7 meters tall. Theearliest modern men were taller (between 1.6 and1.85 meters), but with a brain size approximatingthat of the neanderthaler man (Stringer, 1992).They had less prominent bow ridges and a lessrobust skeleton, longer legs, and the shape of their

8O ALBERT GRAMSBERGEN

hip joints and pubic bone suggest that they movedtheir legs in a modern fashion (Martin, 2002). Theolder fossils of these modern men date back to onehundred thousand years ago, and this indicates thatthe homo neanderthalensis and the modern manhave coexisted for a considerable period. Thespread of these modern humans over Africa, Asia,and Europe seems to have occurred from aroundforty thousand years ago (Stringer, 1992), leavingproducts of their manual skills and artistic talentsat several places, among those in the Cro Magnoncaves in the P6rigord in France.

The question on the relation between theemergence of the bipedal gait and the increase inbrain size has repeatedly been raised in the past.The issue at stake is whether it was the larger brainwith greater motor capacities that has enabled thehominids to keep balance and to move the legs in a

sophisticated fashion, the alternative being that theincrease in brain size followed the development ofbipedal gait. Studying the trends in the bodyweight-brain weight ratios in earlier and morerecent hominids solves this question. The differentvarieties of australopithecines walking bipedally,lived from about four until one million years ago,with brain sizes ranging from 400" to 500 mL(Wood 2002). Only since the emergence of thehomo habilis (about 2 million years ago), alongwith the homo erectus (1.8 million years ago), andthe homo sapiens (from around 100,000 yearsago), has the brain-to-body weight ratio deflectedmore steeply from that in the australopithecinesand in phylogenetically older apes. The 2.5-to 3-fold increase in brain size, from around 500 gramsuntil around 1400 to 1500 grams, was paralleledby a moderate increase in body weight from an

average value of between 40 and 50 kilograms foraustralopithecines to 60 and 70 kilograms inmodern man (Deacon, 2002, Stringer, 2002). Thisobservation implies that the increase in brain size,also coined cephalization, started about twomillion years after hominids started walkingbipedally. Obviously, this trend in brain size is

based upon global approximations, and indicationsfor regional deviations from these trends could notbe considered.

The increases in the dimensions of the skull(because of the larger brain) in conjunction withdecreases in the size of the inner pelvis in morerecent hominids because of the erect gait andchanges in leg movements (see, above) wereamong the factors that induced that term age inhuman babies is at an early stage of braindevelopment and that a relatively large part ofbrain development occurs in babies after they areborn (Deacon, 2002). An additional factor for birthat an early stage is that the metabolic demands ofthe brain mass at later stages of intra-uterinedevelopment cannot be met by the capacity of thematernal placenta. The consequences of a "pre-mature, but physiological" birth at term age, (theterm physiologische Frihgeburt is from Portmann)for behavioral and neurological development werediscussed extensively by Prechtl (1984).

INNERVATION OF TRUNK ANDEXTREMITY MUSCLES

The emergence of extremities, the erect gait,and the possibility to use the hands and fingers formanipulating objects have been paralleled bymorphological changes in muscles, as well as bychanges in fiber type distributions and changes inthe morphology of the skeleton, as well as byimportant changes in the central nervous system.Skeletal fragments and fossils do allow thereconstruction of evolutionary pathways, remainsof tools and artistic expressions suggest a certainstage of manipulative skills, but no traces of braintissue are left. However, comparison ofneuroanatomical details in still existing membersof evolutionary ancient orders, such as fish,amphibians, and reptiles with mammals and trendsin these changes enable to reconstruct globally theevolution that has taken place in brain systems and


circuitries. Within the scope of this essay, a fewrelevant phylogenetic aspects of motor systemswill be discussed.

In fish, propulsion is effected by rhythmic andundulating trunk movements. The vast and detailedinvestigations in the Lamprey by Sten Grillner andhis group (1991) have given insight into the detailsof the neural circuits involved, and similar neuralmechanisms are probably effective in otherfimblessvertebrates. These circuits consist of interactinggroups of excitatory and inhibitory neuronescommunicating with a variety of neurotransmittersand neuromodulators, producing an alternatingactivation and relaxation of the muscles at theright and left side of the trunk. These circuits, oroscillators, in each of the trunk segments havebeen coined Central Pattern Generators (CPGs),and a time-delay in their activation leads to awave-like, rostro-caudal progression of musclecontractions, an undulating movement and by that,to propulsion of the body. Medially descendingprojections from the brain, analogous to thereticulospinal tract (RetST) in mammals inducethe start and halt of these movements, and thesealso can increase and decrease swimming speed bychanging the delay-times between the activation ofthe respective CPGs (Ten Donkelaar, 1982,Grillner et al., 1991).

Amphibians and reptiles live on firm ground,and their four extremities keep the body off theground. In these orders, laterally descending fiberprojections have evolved in the spinal cord, inaddition to the phylogenetically older and mediallydescending projections. The laterally descendingfiber projections activate the motoneurones of theextremity muscles. The projections emerge frombrain stem nuclei at the contralateral side and mostimportant among these are the red nuclei in thebrain stem (giving rise to the rubro-spinal tract,RubST). Its activity in the amphibiae and thereptiliae is superimposed upon the activity in themedially descending systems (Kuypers, 1982),implying that progression in these animals, is

effected by the pattern of trunk movements. Anactivation of the antigravity muscles in theextremities lifts the body and increases theeffectivity of locomotion. Still, some animals areable to make fairly sophisticated leg movements,such as the frog, which, as Ebbeson (1976) hasnoted is able with its hindlegs to remove a grain ofsand from the eye. The medially descending fibersstemming from reticular, vestibular, and tectalnuclei mainly project to the motoneurones of trunkmuscles and the activity in these projections isfunctionally related both to progression andpostural activities (Peterson et al., 1979; Vinay etal., 1998; Vinay et al., 2000).

Quadrupedal mammals have both laterally andmedially descending motor projections in thespinal cord, but the functional importance of thelaterally descending systems (the RubST and alsothe more recent corticospinal tract, the CST) andthe central motor areas involved in steeringextremity movements have drastically increased

(Ten Donkelaar, 1982). Indeed, in quadrupedspropulsion is primarily effected by extremitymovements rather than by trunk movements.

In quadrupeds, the RubST plays an importantrole in activating the extremity muscles involved inlocomotion. The RubST particularly governs theactivation of the proximal extremity muscles asindicated by the localization of the terminal fields ofthe projecting fibers (see Kuypers, 1982 for detailsand references). The red nucleus receives much ofits input from the deep cerebellar nuclei. Electricalrecordings from these nuclei and from the rednucleus in cats have shown electrical activity inphase with walking movements (Orlovsky, 1972).Data from monkeys and the results from a series ofelegant experiments in rats (Whishaw et al., 1986)suggest that the RubST is also involved in skillfulextremity movements. The crossed portion of theCST in quadrupedal animals, other than in man,probably plays a main role in modulating theafferent information as most fibers terminate in thedorsal horn (Porter & Lemon, 1993).


In apes and even more so in man, the CSTemerging from several cortical fields has becomethe most important descending motor tract. TheCST (and particularly the fibers from the primarymotor cortex) allows for the--as Kuypers calledthem--fractionated finger and toe movements byvirtue of monosynaptic connections between corticalneurones and motoneurones in the spinal cord(Lawrence & Kuypers, 1968; Kuypers, 1982).These findings have been corroborated by stimu-lation experiments, by electrical recordings duringhand movements, and by imaging techniques. TheRubST in man might still be involved in theactivation of proximal extremity muscles (Kuypers,1982). However, as the magnocellular part of thered nucleus in man is only small (this specific part isthe source of the RubST in lower vertebrates),others doubt whether this projection in man persistsinto adulthood, and if so, whether it plays an

important role (Holstege, 1991).Rhythmic leg movements, such as those during

walking in quadrupeds and in man, probably are

produced by specialized neural circuits in the brainstem and spinal cord, and these circuits (similar tothose circuits in fish that produce the axial

swimming movements) are known as CPGs(Grillner, 1981, Cazalets et al., 1995, Kjaerulff &Kiehn 1996, Cazalets, 2001). The CPGs for thehindleg movements alternatingly activate leg flexorsand leg extensors; CPGs have been identified at

upper lumbar levels in rats and also in cats, butslightly more caudally. CPGs most probably exist inman as well (Forssberg, 1985, Forssberg & Dietz

1997). Control of an upright and straight postureduring standing or bipedal locomotion, and simul-taneously the performance of arm and hand move-

ments, poses intricate cybernetic problems in man.

To this, CPGs in close cooperation with severalareas in the cerebral cortex, the cerebellum, thebasal ganglia, as well as a strong myelinatedcorticospinal tract and a multitude of ascendingtracts to thalamus and cerebellum are actingtogether with brain stem areas involved in the

control of posture and the maintenance of equili-brium during walking.

POSTURAL CONTROL AND THEDEVELOPMENT OF WALKING

The different phylogenetic ancestries of thetrunk and extremities are reflected in the differenttimescales of the development of the neural systemsunderlying trunk and limb movements, respectively.Studies into the neuro-ontogeny of postural controland the control of movements like walking andreaching indeed have demonstrated that both aspectsfollow separate (although inter-dependent)trajectories. Investigations into reaching by humanbabies in the first years of life, performed byHadders-Algra and her group, have shown that theefficiency and the fluency in the movement

trajectories of the arms are related to the timing andthe extent of adjustments in trunk muscles(Hadders-Algra et al., 1996, Van der Fits et ai.,1999). Postural control changes from a feed-backtype of control with reactions to self-generatedmovements of the reaching arm (or reactions toperturbations) to a feed-forward type of control, inwhich postural adjustments before and during thereaching movement are elements of one integratedmovement program (for details on this developmentas well as on stages therein, see Hadders-Algra, this

issue). Similarly, in the development of free walkingduring the first years of life it appears that thecontrol of posture, as indicated by the ability tostand and to maintain equilibrium during walking isthe limiting factor for an effective and fluentperformance of such tasks.

Also in rats, the development of posturalcontrol and the control of extremity movements

follow different time scales. Altman and his group(Altman & Bayer, 1984) studied the developmentof the spinal cord in rats and demonstrated that themotoneurons for the extremity muscles developabout one day ahead of those for the trunk


muscles. The motoneurones in the cervico-thoracicand lumbo-sacral intumescences innervating therostral and caudal extremities develop on

embryonic day (E)I 2 and E13, whereas those forthe innervation of the trunk muscles are born onlyat El4 or later (rats are born after a gestationalperiod of 21 to 22 days). On the other hand, themedially descending fiber tracts in rats innervatingthe motoneurones of the trunk muscles havereached caudal levels already around El4 (Lakke,1997), whereas the laterally descending systemsdevelop only between week thereafter (theRubST; Lakke, 1997) or still later (the CST; Joneset al., 1982, Joosten et al., 1989, Lakke, 1997). Asto the development of the central structuresinvolved, most information is known on thedevelopment of the cerebellum. The cerebellum isinvolved in adjusting postural control to ongoingmovements (Grillner, 1981, Gramsbergen, 1998,see also Swinny, this issue) and in the fine-tuningof the activity of spinal motoneurones. ThePurkinje cells, the deep cerebellar nuclei (theoutput nuclei) and the so-called precerebellarnuclei (feeding their input to the cerebellum) alldevelop very early in ontogeny. However, granularcells (the most numerous cell type in the brain)with their parallel fibers impinging upon thePurkinje cells develop markedly late. In thehuman, the cerebellar growth spurt occurs fromshortly before birth well into the first year afterbirth (Dobbingm, 1981), but in the rat, this devel-opment takes place completely after birth (Altman& Bayer, 1996). Cortical circuitry in the cere-bellum therefore is established only at a relativelylate stage in the development of motor control.

These few examples illustrate the complicatedtimescales in the development of the neural systemsinvolved in extremity movements (the ’lateralsystem’), in trunk movements (the ’medial system’),and in the cerebellum, which is involved in theintegration of these both aspects (see, below).

Our own research into the ontogenesis of loco-motion in rats sheds further light onto the

functional aspects of movement control. A fewconsiderations point to the rat as the experimentalanimal of choice for neuro-ontogenetic research.Rats are born at an early stage of brain maturation,which allows investigation of the early stages ofdevelopment in their postnatal period. Rats ofaround 13 days after birth might be compared, asthe stage of brain development is concerned withhumans around term age (Romijn et al., 1991, seealso Clancy et al., 2001). In addition, rodents in an

evolutionary sense are relatively modern animals.Taking the CST, the most modern descending fiber

system as an indicator, in rats this tract descendsas far as lumbar levels and at cervical levelsinvades the ventral horn (Jones et al., 1982). It hasbeen suggested that the CST is involved in skilled

forepaw movements (Whishaw & Metz 2002. Inthese respects, rats are more advanced than e.g.,cats or dogs.

Shortly after birth, when rats move from their

position, movement is effected by undulatingmovements of the trunk. Two or three days later, therostral extremities assist in lifting the body from thefloor (Gramsbergen, 1998) and another two or threedays later, the hindlegs also participate in crawling.The rat then still moves by undulating trunkmovements during locomotion very much like thosein adult amphibians (and also resembling those inhuman babies). At the age of about week, rats canstand on their fours and make a few staggeringsteps. The bouts of such walking movementsincrease, but the rats keep moving slowly, oftenwith a tremor in the trunk (Altman & Sudarshan,1975, Westerga & Gramsbergen, 1990, Geisler,1993). At P15, in the course of day, this immaturepattern is replaced by a smooth and adult-likewalking pattern (Westerga & Gramsbergen, 1990).

From then onward, the feet and limbs remainadducted, the fluency and the speed of walkingincrease remarkably, and equally striking are thesudden variations in walking speed that can occur.This transition is accompanied by changes in EMGpatterns of the major hindlimb muscles. Until the


15th day, EMG recordings of the gastrocnemiusmuscles, the soleus, and the tibialis muscles showirregular activity. The gastrocnemius muscle (thelimb extensor) and its antagonist, the tibialisanterior muscle (the flexor), often show simulta-neous activity (Westerga & Gramsbergen, 1993,1994), much like the cocontractions that have beendescribed by Forssberg (1985) in the legs ofhuman babies during "infantile stepping". Afterthe transition into the adult-like walking pattern,clearly delineated EMG bursts occur. A long’tonic’ burst in the gastrocnemius muscle accom-

panies the stance phase, and a brisk burst in thetibialis anterior muscle precedes the onset of theswing phase; the co-contractions in the antago-nistic muscles have disappeared after this shift(Westerga & Gramsbergen, 1993).

At earlier ages, the lateral and medial longis-simus muscles in the back are irregularly activatedduring locomotion. From P16, the medial backmuscles are continuously active during walking andstanding and the laterally located back muscles are

activated in phase with the stepcycle of the hindlegs(Geisler et al., 1997). Then, the muscle is activeduring the contraction of the contralateral gastro-cnemius muscles (i.e. during the stance phase at thatside). During later development, a further rear-

rangement in the activity of the back muscleactivity occurs. From P21, the lateral back muscleis activated during the contraction of the gastro-cnemius muscle at the ipsilateral side, and thisshift possibly relates to an increased efficiency ofsuch coupling (Gramsbergen et al., 1999).

Based on these results, we concluded thatpostural control is the decisive factor in the devel-opment of the adult-like walking pattern. Strongadditional evidence has been obtained in experi-ments in rats subjected to deprivation of part of thevestibular information, by plugging both horizontalsemi-circular canals at P5. Behavioral observationsin these animals indicated that such interferencewith vestibular input leads to a marked retardationin those patterns requiring a high degree of

postural control, such as grooming (retarded byor 2 days) and rearing (standing on the hindlegswithout support) by 4 to 5 days (Geisler et al.,1996). This delay leads to a retardation in thedevelopment of fluent walking by 3 to 4 days(Geisler et al., 1996; Geisler & Gramsbergen, 1998).The activation of the long back muscles in phasewith the hindleg movements, which in normal ratsoccurs around P16), is also delayed by at least 2days. Moreover, this coupling remains highly variablethroughout the observation period of 45 days.

In summary, our results in rats indicate that theneural development of postural control (involvingan intricate feed-forward programming of adjust-ments in ’postural muscles’) is the limiting factorfor the development of fluent type of walking.Similarly, in human babies and in children, feed-forward control of posture, as indicated by specificpatterns of activation of muscles involved inpostural control, is the prerequisite for efficientreaching movements (Hadders-Algra et al., 1996,Van der Fits et al., 1999) and for walking as well(Forssberg & Dietz, 1997).

Many brain structures are inv.olved inprogramming mutual adjustments in the trunk andlimbs during such complex movements. Frombrain pathology in the elderly, it is well known thatanomalies in the basal ganglia seriously interferewith such movements (Visser & Bloem, this issue),but, unfortunately not much is known about thedevelopment of the basal ganglia in man, nor ine.g. rats. Similarly, the sensorimotor cortices mustplay a key role in such adjustments as indicated bythe serious motor impairments occurring afterinternal capsule lesions at the neonatal age. Suchimpairments in the human particularly becomeapparent from the age at which functionalconnections between CST and spinal moto-neurons and interneurons are established.

Cerebellar processing plays an important roleas well in programming the adjustments in trunkand extremity movements during complex motorprograms, or, in coupling postural control to limb


movements (Grillner, 1981, Gramsbergen, 1998).A few arguments for a key role of the cerebellumin these adjustments are the following. Firstly,anatomic data indicate that the cerebellum, morethan any other neural system, is minutely informedon the orientation of the body in space, on thepositions of the body segments in relation to eachother by proprioceptive and vestibular input, andalso indirectly by visual and auditory input(Grillner, 1981, Brodal, 1992). The cerebral motorcortex informs the cerebellum on intendedmovements by massive projections via the pontinenuclei. The effects of motor commands aremonitored by the cerebellum by afferent inputfrom the ventral spinocerebellar tract (conveyinginformation on the activational state of themotoneurones or the status of the motor command)and via the dorsal spinocerebellar tract (conveyinginformation on proprioceptive feedback or, theeffect of the motor command). Based on thisknowledge, it seems highly plausible that thecerebellum plays a key role in adjusting therecruitment of motoneuronal activities.

Secondly, cerebellar anomalies are related to aloss of fluency in movements and to a retardeddevelopment of complex motor patterns likewalking. In Down’s syndrome, in which cerebellardevelopment is both decreased and retarded, thedevelopment of postural control and motor perfor-mance is delayed and often remains suboptimal toa larger or lesser degree (Henderson et al., 1981,Shumway-Cook & Woollacott, 1985). In our own

experiments in rats, we ablated a cerebellarhemisphere at the 2nd, 5th, and 10th days, and atlater ages as well. In animals lesioned until the 10th

day, we demonstrated that motor development untilthe 15th day (the age at which the transition intothe fluent walking pattern normally merges) isnormal, but that this shift did not ccur in ratssubjected to a cerebellar hemispherectomy (fordetails and references, see Gramsbergen, 1998).

Based on these considerations, we suggestedthat, the cerebellum plays a key role in the feed-

forward programming of postural adjustmentsalong with complex movement programs.

EPILOGUE

Postural control in humans is dependent, to alarge extent, upon trunk and neck muscles, as wellas on antigravity muscles in the legs. The discussionabove h as indicated that in vertebrates, the axialmuscles (from fish onward) and their neural controlhave a phylogenetically older history than the flexorand extensor muscles involved in walking and thedistal extremity muscles in manipulating. Data onthe ontogeny of motor control indicate that theskeleto-muscular structures and neural systemsinvolved in postural control develop partly aheadand partly later than the structures and systemsinvolved in steering extremity movements.

The cerebellum obviously has a pivotal role inmutual adjustments in the functioning of thephylogenetically older and newer structures. Froma phylogenetic perspective, it is interesting to notethat the cerebellum increased its relative size fromreptiles onward, particularly in birds and mammals(Crosby, 1969). In higher vertebrates, thecerebellum plays a prominent role in the control ofmovement and in the acquisition of motor skills.The cerebellum develops partly after birth in thehuman and therefore is vulnerable to adverseperinatal influences (such as deficient food supply,prolonged treatment with corticosteroids etc;Gramsbergen, 1998). Both factors seem to justifyfocusing our scientific research efforts on thedevelopment of this structure.

REFERENCES

Aicardi J, Bax M. 1992. Cerebral palsy. In: Aicardi J,ed, Diseases of the Nervous System in Childhood.(Clinics in Developmental Medicine, Nos. 115-118). London, UK" MacKeith Press, OxfordBlackwell Scientific Publications; 330-374


Altman J, Bayer SA. 1984. The development of the ratspinal cord. Adv Anat Embryol Cell Biol 85: 1-164.

Altman J, Bayer SA. 1996. Development of the Cere-bellar System. Boca Raton-New York-London-Tokyo: CRC Press; 1-783.

Altman J, Sudarshan K. 1975. Postnatal developmentof locomotion in the laboratory rat. Anim Behav23: 896-920.

Brodal P. 1992. The cerebellum. In: Bro.dal P, ed, TheCentral Nervous System, Structure and Function.New York, NY, USA: Oxford University Press;262-282.

Cazalets J-R, Borde M, Clarac. 1995. Localization ofthe central pattern generator for hindlimb locomo-tion in newborn rat. J Neurosci 15:4943-4951.

Cazalets J-R. 2001. Development of the neural correlatesof locomotion in rats. In: Kalverboer AF, Grams-bergen A, eds, Handbook of Brain and Behaviourin Human Development. Dordrecht, TheNether-lands: Kluwer; 447-466.

Chatterjee S. 1982. Phylogeny and classification oftheco-dontian reptiles. Nature 295’ 317-320.

Clancy B, Darlington RB, Finlay BL. 2001. Translatingdevelopmental time across mammalian species.Neuroscience 105:7-17.

Crosby EC. 1969. Comparative aspects of cerebellarmorphology. In: Llinfis R, ed, Neurobiology ofCerebellar Evolution and Development. Chicago,Illinois, USA: AMA; 19-42

Deacon TW. 2 002. The human brain. In: Jones S,Martin R, Pilbeam D, eds, The CambridgeEncyclopedia of Human Evolution. Cambridge,UK: Cambridge University Press; 115-121.

Dobbing J. 1981. The later development of the brainand its vulnerability. In: Davies JA, Dobbing J;eds, Scientific Foundations of Paediatrics, 2na ed.London, UK: William Heinemann; 744-758.

Dover G. Anti Dawkins. 2000. In: Rose H, Rose S, eds,Alas, Poor Darwin, Arguments Against Evolu-tionary Psychology. London, UK: Jonathan Cape;47-66

Ebbeson SOE. 1976. Morphology of the spinal cord.In: Llinfis R, Precht W, eds, Frog Neurobiology.Heidelberg, Germany: Springer; 679-706.

Fleagle JG. 2002. Primate locomotion and posture. In:Jones S, Martin R, Pilbeam D, eds, The CambridgeEncyclopedia of Human Evolution. Cambridge,UK: Cambridge University Press; 75-79.

Forssberg H. Ontogeny of human locomotor control.1985. I. Infant stepping, supported locomotion

and transition to independent locomotion. ExpBrain Res 57: 480-493.

Forssberg H, Dietz V. 1997. Neurobiology of normaland impaired locomotor development. In: ConnollyKJ, Forssberg H, eds, Neurophysiology and Neuro-psychology of Motor Development. London, UK:MacKeith Press; 78-100.

Geisler HC, Westerga J, Gramsbergen A. 1993.Development of posture in the rat. Acta NeurobiolExp 53:517-523.

Geisler HC, Westerga J, Gramsbergen A. 1996. Thefunction of the long back muscles during posturaldevelopment in the rat. Brain Behav Res 80:211-215.

Geisler HC, Van der Fits IBM, Gramsbergen A. 1997.The effects of early vestibular deprivation on themotor development in the rat. Brain Behav Res86: 89-96.

Geisler HC, Gramsbergen A. 1998. Motor developmentafter vestibular deprivation in rats. NeurosciBiobehav Rev 22: 565-569.

Geisler HC, Gramsbergen A. 1998. The EMGdevelopment of the longissimus and multifidusmuscles after plugging the horizontal semicircularcanals. J Vestib Res 8: 399-409.

Gould SJ. 2000. More things in heaven and earth. In:In: Rose H, Rose S, eds, Alas, Poor Darwin,Arguments Against Evolutionary Psychology.London, UK: Jonathan Cape; 85-105.

Gramsbergen A. 1998. Posture and locomotion in therat: independent or interdependent development?Neurosci Biobehav Rev 22: 547-553,.

Gramsbergen A, Van Eykern LA, Taekema HC,Geisler HC. 1999. The activation of back musclesduring locomotion in the developing rat. BrainRes Dev Brain Res 112: 217-228.

Grillner S. 1981. Control of locomotion in bipeds,tetrapods and fish. In: Brookhart JM, MountcastleVB, eds, Handbook of Physiology Section I, TheNervous System, Volume II part 2. MotorControl. Bethesda Maryland, USA: AmericanPhysiology Society; 1179 -123.

Grillner S, Wall6n P, Brodin L, Lansner A 1991.Neuronal network generating locomotor behaviourin lamprey: circuitry, transmitters, membraneproperties, and simulation. Ann Rev Neurosci 14:169-199.

Hadders-Algra M. Development of postural controlduring the first 18 months of life. Neural Plast 2 0:27-36.


Hadders-Algra M, Brogren E, Forssberg H. 1996.Ontogeny of postural adjustments during sitting ininfancy: variation, selection and modulation. JPhysiol (Lond) 493:273-288

Henderson S, Morris J, Frith U. 1981. The motordeficit in Down’s syndrome children: a problemoftiming? J Child Pyschol Psychiatr 22: 233-245.

Holstege G. 1991. Descending motor pathways andthe spinal motor system: limbic and non-limbiccomponents. Prog Brain Res 87:307-421

Jones EG, Schreyer DJ, Wise SP. 1982. Growth andmaturation of the rat corticospinal tract. ProgBrain Res 57: 361-379.

Joosten EA, Gribnau AA, Dederen PJ. 1989. Postnataldevelopment of the corticospinal tract in the rat.An ultrastructural anterograde HRP study. AnatEmbryol 179: 449-456.

Kjaerulff O, Kiehn O. 1996. Distribution of networksgenerating and coordinating locomotor activity inthe neonatal rat spinal cord in vitro: a lesionstudy. J Neurosci 16: 5777-5794.

Kuypers HG. 1982. A new look at the organization ofthe motor system. Prog Brain Res 57:381-403.

Lakke E. 1997. The projections to the spinal cord ofthe rat during development: a timetable ofdescent. Adv Anat Embryol Cell Biol 135: 1-143.

Lawrence DG, Kuypers HG. 1968. The functionalorganization of the motor system in the monkey.I. The effects of bilateral pyramidal lesions. Brain91: 1-14.

Leakey MG, Feibel CS, McDougall I, Walker A.1995. New four-million-year.old hominid speciesfrom Kanapoi and Allia bay, Kenya. Nature 376:565-571.

Martin R. 2002. Walking on two legs. In: Jones S,Martin R, Pilbeam D, eds, The CambridgeEncyclopedia of Human Evolution. Cambridge,UK: Cambridge University Press; 78.

Orlovsky GN. 1972. The effect of different descendingsystems on flexor and extensor activity duringlocomotion. Brain Res 40: 359-371.

Peterson BW, Pitts NG, Fukushima K. 1979. Reticulo-spinal connections with limb and axial moto-neurones. Exp Brain Res 36" 1-20.

Porter R, Lemon R. 1993. Corticospinal function andvoluntary movement. Monographs of the Physio-logical Society, vol 45. Oxford, UK; ClarendonPress; 1-428.

Prechtl HFR. 1984. Continuity and change in early neuraldevelopment. In: Prechtl HFR, ed, Continuity of

Neural Functions from Prenatal to Postnatal Life.Clinics in Developmental Medicine 94; Oxford,Blackwell Scientific Publishers Ltd; 1-15.

Reisinger E. 1926. Untersuchungen am Nervensystemder Bothrioplana semperi. Z Morphol tkol Tiere;5:119-149.

Romer AS. 1969. Vertebrate history with specialreference to factors related to cerebellar evolution.In: Llinis R, ed, Neurobiology of CerebellarEvolution and Development. Chicago, Illinois,USA: American Medical Associaton; 1-18.

Romijn HJ, Hofman MA, Gramsbergen A. 1991. Atwhat age is the developing cerebral cortex of therat comparable to that of the full-term newbornhuman baby? Early Hum Dev 26:61-67.

Shumway-Cook A, Woollacott M. 1985. Dynamics ofpostural control in the child with Down syndrome.Physical Ther 65" 1315-1322.

Stringer CB. 2002. Evolution of early humans In:Jones S, Martin R, Pilbeam D, eds, The CambridgeEncyclopedia of Human Evolution. Cambridge,UK: Cambridge University Press; 241-251.

Swinny JD, van der Want JJL, Gramsbergen A. 2005.Cerebellar development and plasticity: perspectivesfor motor coordination strategies, for motor skills,and for therapy. Neural Plast 20: 81-88.

Ten Donkelaar HJ. 1982. Organization of descendingpath-ways to the spinal cord in amphibians andreptiles. Organization of descending pathways tothe spinal cord in amphibians and reptiles. ProgBrain Res 57: 25-67.

Van der Fits IBM, Otten E, Klip AWJ, Van EykernLA, Hadders-Algra M. 1999. The development ofpostural adjustments during reaching in healthyinfants aged 6-18 months: evidence for twotransitions. Exp Brain Res 126: 517-528.

Vinay L, Bussieres N, Shupliakov O, Dubuc R, GrillnerS. 1998. Anatomical study of spinobulbar neuronesin lampreys. J Comp Neurol 397: 475-492.

Vinay L, Brocard F, Pflieger JF, Simeoni-Alias J,Clarac F. 2000. Perinatal development of lumbarmoto-neurones and their inputs in the rat. BrainRes Bull 53:635-647.

Visser JE, Bloem BR. Role of the basal ganglia inbalance control. Neural Plast 20:89-101.

Ward CV, Leakey MG, Walker A. 2001. The earliestknown australopithecus, A. anamensis. J HumanEvolut 41:255-368.

Westerga J, Gramsbergen A. 1990. The development oflocomotion in the rat. Dev Brain Res 57: 163-174.


Westerga J, Gramsbergen A. 19 93. Changes in theEMG of two major hindlimb muscles duringlocomotor development in the rat. Exp Brain Res92: 479-488.

Westerga J, Gramsbergen A. 1994. Development ofthe EMG of the soleus muscle in the rat. DevBrain Res 80: 233-243.

Whishaw IQ, O’Connor WT, Dunnett SB. 1986. Thecontributions of motor cortex, nigrostriataldopamine and caudate-putamen to skilled tbre-limb use in the rat. Brain 109:. 805-843.

Whishaw IQ, Metz GA. 2002. Assessment of the

pyramidal tract contribution to skilled movement inthe rat: Absence of impairments or recoverymediated by the uncrossed pyramidal tract in the ratversus enduring deficits prodced by the crossedpyramidal tract. Behav Brain Res 134:323-336

White TD, Suwa G, Asfaw B. 1994. Austraolo-pithecus ramidus, a new species of early hominidfi’om Aramis, Ethiopia. Nature 371: 306-312.

Wood BA. 2002. Evolution of australopithecins In: JonesS, Martin R, Pilbeam D, eds, The CambridgeEncyclopedia of Human Evolution. Cambridge, UK:Cambridge University Press; 231-240.

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