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566 Developmental Medicine & Child Neurology 2000, 42: 566572

The Neuronal GroupSelection Theory: aframework to explain

variation in normalmotor development

Mijna Hadders-Algra MD PhD, Movement and DevelopmentGroup, Department of Medical Physiology, University ofGroningen, Groningen, The Netherlands.

Correspondence to author atUniversity HospitalGroningen, Developmental Neurology, CMC-IV, 3rd floor,Hanzeplein 1, 9713 KZ Groningen, The Netherlands.E-mail: [email protected]

During the last century, knowledge of the mechanisms gov-erning the functions of the central nervous system increasedrapidly as sophisticated physiological, neurochemical, andimaging techniques developed. In the field of motor control,better understanding of neurophysiology caused a gradualshift from the concept that motor behaviour is largely con-trolled by reflex mechanisms1,2 towards the notion thatmotility is the net result of complex spinal or brainstem activ-

ity, which is subtly modulated by segmental afferent informa-tion and ingeniously controlled by supraspinal networks3,4.Nowadays it is assumed that motor control of rhythmicalmovements like locomotion, respiration, sucking, and masti-cation is based on so-called central pattern generators(CPGs): neuronal networks which can generate complexbasic activation patterns of the muscles without any sensorysignals. Nevertheless, sensory information of the movementis important in adapting the movement to the environment.The activity of the networks, which are usually located in thespinal cord or brainstem, is controlled from supraspinalareas via descending motor pathways4. The supraspinalactivity itself is organized in large-scale networks in which

cortical areas are functionally connected through directrecursive interaction or through intermediary cortical orsubcortical (striatal, cerebellar) structures57.

Concurrently, albeit at a considerably slower pace, knowl-edge of motor development has increased. Consequently,theoretical frameworks for the processes involved in thedevelopment of motor control have changed. The aim of thepresent paper is to discuss the two major current but con-flicting theories; the Neural-Maturationist Theories and theDynamic Systems Theory. A third theory, the NeuronalGroup Selection Theory (NGST) will also be discussed. TheNGST combines the nature part of the Neural-MaturationistTheories with the nurture part of the Dynamic Systems

Theory. Application of the concepts of the NGST could facili-tate the understanding of motor disorders and, thereby, offernew possibilities for intervention therapies an issue which

will be discussed in a forthcoming publication8.

The Neural-Maturationist Theories

In the mid-1900s, motor development was generally regard-ed as a gradual unfolding of predetermined patterns in the

central nervous system9. Gesell and Amatruda claimed thatmaturation is the net sum of the gene effects operating in aself-limited time cycle10 (p 20), a concept which virtually leftno place for interaction with the environment11. The ideathat behavioural patterns emerge in an orderly geneticsequence, resulted in the recognition of general develop-mental rules, such as the cephalocaudal and central-to-distalsequences of development. These notions prompted thepioneering work developmental diagnosis, consisting ofneat series of tests for the assessment of developmental mile-stones11. Motor development was considered to be theresult of an increasing cortical control over lower reflexes.Or, as Peiper expressed it, at birth the various brain portions

do not function equally well; rather, their function startsfrom the midbrain and continues to the cerebral hemi-spheres, which at birth are still neurologically inactive.Therefore, they have no inhibitory influence on the deepercerebral portion and as a consequence the reflexes of themidbrain are not suppressed and become manifest.12

(p 149). Peiper was convinced that basic motor skills, such asstanding and walking, are not learned by experience but arethe result of cerebral maturation. He illustrated this idea withthe case report of a girl who at the age of 6 months was putinto a plaster cast because of bilateral congenital hip disloca-tion. She remained in the cast, which prevented standingand walking, until she was 18 months old. The cast was then

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replaced by a half cast. One day after the introduction of thehalf cast, the girl freed herself from it. Immediately she start-ed to walk, erect and unaided12 (p 233).

Another pioneering developmentalist, usually classifiedas a Neural-Maturationist, is McGraw. Her research peaked inthe 1930s and 1940s, i.e. when Neural-Maturationist ideas

were dominant. McGraw believed that infant motor develop-ment was not entirely commanded by endogenous rules13.She tested her ideas with a remarkable experiment on a pair

of twins (who were probably dizygotic)14. The first-borntwin, Johnny, showed signs of transient hypotonia during thefirst postnatal months. He was provided with intensive age-specific motor practice from early life until the age of 2 years.On the contrary, spontaneous motor activity of his neurolog-ically normal brother, Jimmy, was relatively restricted, as he

was confined to his crib for most of the day during the exper-imental period. Despite Johnnys neurological dysfunction,resulting in a slight disadvantage in the development of sit-ting and standing, the study showed that both boys obtainedmost motor milestones, such as the onset of reaching, crawl-ing, and walking; the disappearance of the palmar graspreflex; and the disappearance of the Moro reaction, at identi-

cal ages. Continued motor training of Johnny after the onsetof independent locomotion at the age of 9 months dramati-cally affected the development of Johnnys motor skills. Hecould rollerskate, climb on steep surfaces and high stools

well before the age of 2 years, skills which Jimmy and his non-restricted peers had not attained at such an early age.McGraw attributed the relative catch-up in motor develop-ment of Johnny during infancy to his training. But she alsorealized that Johnnys training did not result in the immenseacceleration of motor development. She concluded that theeffect of stimulation could only occur within the develop-mental framework set by nature or, as she wrote, a certainamount of neural maturation must take place before anyfunction can be modified by specific stimulation13. Thus,

McGraw considered motor development to result fromnature and nurture, implying that she is not a pure Neural-Maturationist (cf. ref.15).

Dynamic Systems Theory

Thelen et al. were not satisfied with the Neural-MaturationistTheories: How can the timetable of motor solutions beencoded in the brain or in the genes? (p 81)16. They embracedthe ideas of Kugler et al., and Schner and Kelso17,18. Thesescientists followed Bernsteins lines of thought19, who tried tounderstand how the nervous system solves the problem ofmotor coordination. Bernstein realized that the productionof coordinated movements in a body consisting of hundreds

of muscles and joints required specific computational tech-niques of the nervous system. The ideas of Kugler andcoworkers, known as the Dynamic Systems Theory, is basedon the principles of non-equilibrium thermodynamics; sys-tems which maintain energy by interaction with the environ-ment thus creating globally stable structures over extendedperiods of time20. According to Dynamic Systems Theory, pat-terns of behaviour, such as the typical smooth andstraight tra-

jectory of a reaching movement of an adult, act as attractors.This means that a specific type of behaviour, which resultsfrom the effects of (1) its multiple component parts, such asmuscle strength, body weight, postural support, the infantsmood, and brain development, and (2) the effect of

environmental condition and task requirements, spontaneouslyadopts a specific organization2123. Due to the properties ofdynamic pattern formation, continuously occurring changesof the above mentioned component parts or changes of theenvironment or task can induce discontinuous changes(transitions) in behaviour. Thelen et al. argue that develop-ment can be regarded as a dynamic system. Thus, develop-ment is considered to be a self-organizing process, or inThelens words a series of states of stability, instability, and

phase shifts in the attractor landscape, reflecting the proba-bility that a pattern will emerge under particularconstraints16 (p 84). The Dynamic Systems Theory and theNeural-Maturationist Theories differ especially in their viewon the role of the nervous system in motor development.The Neural-Maturationist Theories consider the matura-tional state of the nervous system as the main constraint fordevelopmental progress, whereas in the Dynamic SystemsTheory the neural substrate plays a subordinate role.

Neuronal Group Selection Theory

One of the principle properties of normal development isvariation2426. Variation is present in practically all develop-

mental parameters, such as motor performance, develop-mental sequence, or the duration of developmental stages.But variation is not always equally abundant. Sporns andEdelman attempted to explain the variability in development

with the Neuronal Group Selection Theory27,28. According tothe NGST, the brain, or more specifically, the ensemble ofcortical and subcortical systems is dynamically organizedinto variable networks, the structure and function of whichare selected by development and behaviour. The units ofselection are collections of hundreds to thousands of strong-ly interconnected neurons, called neuronal groups, whichact as functional units. The NGST states that developmentstarts with primary neuronal repertoires, with each reper-toire consisting of multiple neuronal groups. The cells and

the gross connectivity of the primary repertoires are deter-mined by evolution. The repertoires are variable because ofthe dynamic epigenetic regulation of cell division, adhesion,migration, death, and neurite extension and retraction2931.Development proceeds with selection on the basis of affer-ent information produced by behaviour and experience. Theselection process is thought to be mediated by changes insynaptic strength of intra- and intergroup connections, in

which the topology of the cells32 and the presence orabsence of coincident electrical activity in pre- and postsy-naptic neurons play a role29,33. When the selection has justbeen accomplished, behavioural variation is slightly reduced.Soon, however, abundant variation returns because the

organism and its populations of neurons is constantlyexposed to a multitude of experiences. The experientialafferent information induces modifications in the strength ofthe synaptic connections within and between the neuronalgroups resulting in the variable secondary repertoire. Thechanged connectivity within the secondary repertoireallows for a situation-specific selection of neuronal groups.Thus, the secondary neuronal repertoires and their associat-ed selection mechanisms form the basis of mature variablebehaviour which can be adapted to environmental con-straints.

The NGST could end the continuing naturenurturedebate, as the theory explicitly states that development is

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neither exclusively governed by a genetically dictated neuralsubstrate nor by environmental conditions. On the contrary,the theory highlights the notion that development is theresult of a complex intertwining of information from genesand environment. Similar ideas, be it without the concept of

variation and selection, had already been proposed byWaddington34 and Gottlieb35. Gottlieb drew special atten-tion to the role of species- and age-specific behaviour, whichcould play a directing or canalizing role in motor develop-

ment by exposing the individual to specific experiences. Thepresence of such age-dependent canalizing behaviour hadalready been noted by McGraw13 and Peiper12, who bothreported that children exhibit an indomitable urge to exer-cise a function as soon as it emerges. This remarkable driveto exercise a newly developing function emphasizes theimportance of self-produced activity for the creation of opti-mal neuronal circuitries (cf. refs 36, 37).

Neuronal Group Selection Theory and normal motor

development

Translating concepts of the NGST to the domain of humanmotor development results in a developmental progress

with two different phases of variability (Fig. 1).

PRIMARY VARIABILITY

Motor development starts during early fetal life with thephase of primary variability, which continues during infan-cy. Initially it was believed that motor behaviour at early age

was primitive, reflex-based, and monotonous12,38. However,the opposite is true. Detailed studies of motor behaviour offetuses and newborn infants have shown that motility at earlyage is characterized by profuse variation, apparent in move-ment trajectories, and in temporal and quantitative aspectsof motility22,3945, for example. These variations in motoractivity are not neatly tuned to environmental conditions,but actually constitute a fundamental developmental phe-

nomenon. It is conceivable that the abundant variation inmotility is prompted by activity of the epigenetically deter-mined and grossly specified supraspinal primary neuralrepertoires. The system of primary repertoires presumablyexplores, by means of self-generated activity and conse-quently also by means of self-generated afferent information,all motor possibilities available within the neurobiologicaland anthropometric constraints set by evolution.

The properties of primary variability are very well illustrat-ed by general movements (GMs). GMs are the most frequent-ly used movement pattern of the human fetus and newborninfant. They consist of series of gross movements of variablespeed and amplitude, which involve all parts of the body but

lack distinctive sequencing46,47

. Likewise, the muscle coordi-nation patterns of normal GMs are typified by variation inwhich muscles participate, and in the timing and the quantityof muscle activation43,38. Presumably, the rich variation andcomplexity of human GMs reflect the explorative activity of a

widely distributed (sub)cortical network the primary neu-ronal group on the extensive CPG networks of the GMslocalized in the spinal cord and brainstem. The hypothesisthat primary networks located at (sub)cortical level play adominant role in the generation of the primary variability ofGMs is supported by three pieces of evidence. Firstly, gener-alized movements of chicken embryos animals with rela-tively simple supraspinal systems have been described as

monotonous and lacking rotatory components49, whereascomplexity and rich variation in movement trajectory,including rotatory movements are the hallmark of normalhuman GMs47. Secondly, the motility of anencephalic fetus-es, in whom (sub)cortical tissue is entirely absent, is devoidof any variation and complexity50. Thirdly, human GMs,

which lack complexity and variation, i.e. GMs which are defi-nitely abnormal are strong indicators of the development ofcerebral palsy47,48,51,52. The above also implies that the tradi-

tional idea that (sub)cortical areas do not function in new-born infants (e.g. refs 12, 14) is not valid.

GMs are present until about 4 months of postterm age.They are then gradually replaced by goal-directed move-ments. In terms of neural networks, the gradual change fromgeneral movement activity into goal-directed behaviourcould mean that the widely distributed (sub)cortical net-

works controlling GM activity are flexibly rearranged bymeans of changed synaptic connectivity into multiple small-er networks (cf. ref.53). In other words, the large (sub)corti-cal GM network is cut into various smaller networks. Thesesmaller (sub)cortical networks form the primary neuronalrepertoires for the control of specific motor behaviours, such

as goal-directed motility of the arms and the legs, and postur-al control. Due to the dissolution of the primary neuronalnetwork of the GMs, their development does not include atransition from a primary to a secondary neuronal reper-toire. This underscores the unique position of GMs inhuman motor development, and supports the notion thatthe (sub)cortical networks involved in the control of GMactivity form the neural building blocks for later motor skills.

All forms of goal-directed motor behaviour start duringinfancy with the phase of primary variability. This is the timeof life when (cortical) synaptogenesis is abundant54,55.The resulting multifarious primary networks enable themost appropriate circuitries to be selected. Indeed, ample

variation characterizes the first phases of reaching and grasp-

ing behaviour22,56,57, of crawling5860, of locomotor motili-ty21,41,61,62, and of postural control44,63,64. The neural systemsdedicated to a specific function explore, during the phase ofprimary variability, all motor possibilities available for thatspecific function. The exploration and continuous process-ing of the concomitant afferent information gradually resultin the selection of the most efficient movement patterns.

SELECTION

The timing of the selection process appears to be functionspecific. During reaching, the selection of a straighter for-

ward-directed arm movement takes place during the secondhalf year after birth22,56,57. Adult reaches usually consist of

one movement unit, i.e. one acceleration and one decelera-tion65. When infants of 4 to 5 months start to reach and graspthey show a variable repertoire of reaching movements,

which vary from rather straight movements of one or twomovement units to multi-unit, tortuous reaching move-ments22,56. Around the age of 7 to 8 months, infants start toselect a reaching movement of two movement-units; a largetransport unit, and a small adjusting unit. The single-unitreach only emerges at the age of 2 years66.

The early phases of the development of postural adjust-ments are also characterized by extensive variation, although

within the limits set by the primary neuronal repertoire, i.e.the epigenetically determined boundaries of direction speci-



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postural adjustments lasts for about 112 to 2 years, whereasthe phase of reduced variation in locomotor coordinationduring crawling is so short that the phase of primary variabil-ity imperceptibly passes into the phase of secondary variabil-ity60,79. The relatively long duration of the reduced variationphase in the domain of postural control could be related tothe difficulty of the task of balancing the body during the firstphases of standing and walking. After the transient phase ofreduced variation, the phase of secondary variability or

adaptive variability starts26,79.

SECONDARY OR ADAPTIVE VARIABILITY

The creation of the secondary (sub)cortical repertoires isassociated with extensive synapse rearrangement, the netresult of synapse formation and synapse elimination54,55,80.It is facilitated by increasingly shorter processing times

which can be attributed in part to ongoing myelination81,82.The long duration of the (sub)cortical developmentalprocesses implies that it takes many years and experiencesbefore the secondary neuronal networks are able to producean efficient motor solution for each specific situation26,83,84.This means that when children are tested in a novel condi-

tion, it takes considerable experience before they are able toadjust perfectly their motor behaviour to the new situation.As laboratory testing in general does not include ample prac-tice, most experimental tests reveal that children show non-optimally adapted motor behaviour with substantial

variation. The amount of variation is inversely related to ageand reaches small adult values first in adolescence8588.

An example of the returning variation after the phase ofthe selection-induced reduced variation can be found in thestudies on postural adjustments during sitting. After the ageof 2 to 3 years, children use those postural adjustments lessfrequently in which all direction-specific neck, trunk, andproximal leg muscles are activated. Instead, they have arepertoire of adjustments in which one, two, or three of the

direction-specific muscles are activated in concert. Withincreasing age, the variable activity can be more preciselyand more efficiently adapted to the specific details of the pos-tural perturbation, such as the sitting position or the size ofthe perturbation79.

The mature situation of the healthy adult is characterizedby an ability to adapt each movement exactly and efficientlyto task-specific conditions or, in the absence of tight con-straints, by the ability to generate multiple solutions orstrategies for a single motor task (e.g. refs 8991). Specificpractice reduces the amount of secondary variation by induc-ing selection of the most efficient strategy out of the reper-toire of adaptive motor strategies92,93. The absence of

practice produces the reverse, it is associated with anincrease in motor variation94.

Conclusion

Applying concepts of the NGST sheds new light on motordevelopment. According to the NGST, variation is the key-

word for normal development. The variation is not random,but determined by criteria set by genetic information34,35.The variation has two forms: primary variability, which is notgeared to external conditions, and secondary variability, in

which motor performance can be adapted to specific situa-tions. In both cases, selection on the basis of afferent infor-mation plays a significant role. Thus sensory information has

an important function in motor development. Presumably,the role of sensory information in motor development islarger than previously presumed on the basis of studies onmotor control in deafferented adult participants65.

Accepted for publication 31st March 2000

AcknowledgementsThanks to Eva Brogren, Tineke Dirks, and the reviewers for their

valuable criticism of the manuscript. Jolanda Schaap is gratefullyacknowledged for technical assistance.

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Mac Keith Meetings

Clinical Neuropsychiatry of Childhood (Open meeting)

Royal Society of Medicine, London, UK. September 11, 2000

Organized by Michael Prendergast. Speakers (in order of

appearance) will include: Professor Eric Taylor, Dr ThierryDeonna, Professor Christopher Gillberg, Professor PeterSzatmari, Dr Isabel Hayman and Professor David Taylor.Professor Alwyn Lishman and Professor Brian Neville willchair the morning and afternoon sessions respectively.

Management and Treatment of Autism (Open meeting)

Royal Society of Medicine, London, UK. October 5, 2000

Organized by Dr Gregory OBrien and Dr Claire Burns.Speakers (in order of appearance) will include: ProfessorMary Coleman, Dr Peter Sullivan, Dr Tom Berney, DrOBrien, Dr Burns, Dr Jane Shields, and Dr Rita Jordan.There will be a panel discussion led by Mary Coleman at

the end of the afternoon

What Obstetricians Can Do to Prevent Disability (Open

meeting)

Royal Society of Medicine, London, UK. October 23, 2000

Organized by Martin Bax. Speakers will include ProfessorLord Winston, Chair of The Little Foundation.

For further information, and to book places at openmeetings, contact Vesna Milenkovic, CME Department, TheRoyal Society of Medicine, 1 Wimpole St, London W1M 8AE.Tel: 0207 290 2988E-mail:[email protected]

Documents

The Neuronal Selection Theory (1)