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NEURAL PLASTICITY VOLUME 10, NO. 1-2, 2003

Development ofAction and the Clinical Continuum

Brian Hopkins

Department ofPsychology, Lancaster University, Lancaster LA1 4YF, England

ABSTRACT KEYWORDS

The development of action is depicted asconsisting of changes in the task-specificcouplings between perception, movement, andposture. It is argued that this approach mayprovide a much needed basis from whichattempts can be made at theoretically unifyingthe constituents of the clinical continuum (viz.,early detection, diagnosis, prognosis, andintervention). Illustrative examples germane tothis approach are given with regard to howposture serves as a constraint on the emergenceof reaching movements and how corticaldevelopment influences the coordination of legmovements as revealed by a study involvinginfants with white matter lesions. Particularattention is paid to early detection and it isrecommended that further improvements tothis aspect of the clinical continuum can bederived from combining serial qualitative andquantitative (kinematic) assessments withbrain-imaging techniques. It is emphasized thatquantitati:.’e assessments should incorporateexperimental manipulations of perception,movement or posture during transitionalperiods in development. Concluding commentsinclude consideration of the timing of earlyintervention.

Reprint requests to: Brian Hopkins, Department ofPsychology, Lancaster University, Lancaster LA1 4YF,England

corticospinal tracts; leg movements; motor equiva-lence; periventricular leukomalacia; ontogeneticadaptations; reaching movements

A. INTRODUCTION

More than 60 years ago, the Germanneurologist, von Weizs/icker (1940/1973), presentedhis Gestalt Circle Theory. The central tenet of histheory was that perception and action areinseparably linked at both the neural and behaviorallevels of organization. Furthermore, the ’circle ofcausality’ between perception and action could onlybe broken by pathological conditions that affectedthe functioning of the brain. Given that at the time,perception and movement control were studied inrelative isolation from each other, these were indeedbold statements not shared by more empiricallyminded students of human behavior, with thepossible exception ofBemstein (1967).

Turning to more recent times, von Weizs/icker’s

tentative claims have resurfaced in theoreticalattempts to capture the mutual reciprocity betweenperception and action at both the level of behavior(for example, Gibson, 1975) and brain architecture(for example, Edelman, 1987). In addition, there is

growing support for his claim that (cortical) brainpathology can result in the dissociation between(visual) perception and the goal-directed movementsthat constitute action (for example, see Milner &Goodale, 1995). Such theorizing has also begun tomake significant inroads into research on

(C) 2003 Freund & Pettman, U.K. 15

16 BRIAN HOPKINS

development, especially during the period ofinIhncy (an excellent example of which can befound in the work of Adolph [1997] on thedevelopment of locomotion). What is lacking sofar, however, in this approach to early develop-ment is to account for the changing relationshipnot only between perception and action but alsobetween them and posture. In the context of earlydetection in particular, it is argued that changes inthe functional relations between perception, move-ment, and posture in the development of action ineedto be accounted for if further improvements are tobe made to this first stage of the clinical continuum.

In what follows, there is a brief overview ofwhat comprises the clinical continuum and whichraises the issue what is meant by ’normality’.Then, consideration will be given to the strengthsand weaknesses of current methods of earlydetection, which are largely based on thequalitative or quantitative analyses of spontaneousor elicited movement patterns. Subsequently, thefindings of two studies considered to be relevant to

improving the potential of early detection are

reviewed. One considers how the control ofposture and movement cohere in the emergence ofreaching and the other the link between (proprio-)perception, and movement in the developmentspontaneous kicking. The latter two-part study alsobrings with it some insights into the developmentof the corticospinal tracts. Finally, concludingremarks include the suggestion that a perception-action approach as outlined here may provide thebeginnings of a framework that can theoreticallyunify all aspects ofthe clinical continuum.

B. THE CLINICAL CONTINUUM

The provision of appropriate forms oftherapeutic intervention for children with major orminor disabilities represents the end point of aseries of interconnected clinical endeavors. These

CLINICAL CONTINUUM

EARLY qualilative/calegoricalDETECTION methods

,who i,s, at risk? quantitative/dimensionalmethods

I DIAGNOSIS- c’mrbidilywhy?

Iwhat is probable

,.urse & outcome?

NTERVENTIO secondary| what be

..._O._.one aboutit._ lertiary

Fig. 1" The clinical continuum that contains a sequence ofinterrelated aspects, but with each one addressing aparticular question. Topics relevant to each aspectthat are discussed in the text are referred to on theright hand side of the figure. The continuumrepresents an ideal sequence of clinical activitiesstarting with early detection and proceedingthrough diagnosis and prognosis to therapeuticintervention. Sometimes both prognosis and inter-vention may follow on from early detection(without diagnosis) as indicated by the thin arrow-headed lines. In these instances, primary inter-vention is the goal in an attempt to prevent theprobable occurrence of some later emerginggeneral disorder (for example, cerebral palsy orcognitive deficits in preterm infants).

other undertakings encompass early detection,diagnosis and prognosis and, together with inter-vention, form the clinical continuum (see Fig. l).

Definitions of these four aspects of the clinicalcontinuum as well as the main issues that confronteach of them are given in Table 1. Where possible,reference is made to how they impinge uponresearch with clumsy children.

DEVELOPMENT AND THE CLINICAL CONTINUUM 17

TABLE 1

Aspect

Earlydetection

Diagnosis

Prognosis

Intervention

Definitions of the four aspects making up the clinical continuum, the main issues facinghow each aspect is put into practice, and comments relevant to these problems

Definition

Identification ofthose individuals at riskfor a functional disorder later indevelopment

1. Assignment of an individual ordisorder to class within taxonomy(e.g.DSM-IV; ICD 10)

2. Determining cause(s) of disorder (whya person is likely to have it)

3. Three typesa. Clinical diagnosis based on signs andsymptoms

b. diagnosis by exclusion: ruling out allbut one disease thought to bedeterminant

c. differential diagnosis: identifyingwhich oftwo or more diseases withsimilar signs or symptoms isdeterminant

Making predictions about the probabledevelopmental course and outcome ofindividual diagnosed with particulardisorder

1. Treatment designed to prevent,ameliorate, or overcome signs andsymptoms associated with disorder2. Three types:a. primary intervention: reducing

incidence of disorder before it occursb. secondary intervention: treating

disorder while it is becomingestablished

c. tertiary intervention: treatingdisorder after it is established

Issues involved1. How early indevelopment forreliable identification?

2. What is child at riskfor?

1. Comorbidity problem:many disorders are notdiscrete categories.Thus:

2. Difficult to distinguishbetween primary andsecondary disorder

3. In such instances, a.and b. types ofdiagnosis are notapplicable

1. For clumsy children:do they ’grow out of it’or does it continue upto and beyondadolescence?

2. Comorbidity problem:which disorder mostdictates course andoutcome?

1. Does interventionresult in predictedeffect?

2. For how long are theeffects sustained afterintervention stops?

3. Does interventionavoid any iatrogeniceffects?

Comment

Claim that a valid functionally basedinstrument available for use in theprenatal period (Prechtl, 1999)

1. Classifying child as clumsy relieson diagnosing signs (standardizedtest performance) and symptoms(from subjective judgments madeby parents and/or teachers using aquestionnaire)

2. Diagnosis of cerebral palsycomplicated because 17% to 60%of such cases have no evidentperinatal or neonatal etiology(Stanley eta., 2000)

Suggestion that isolated GM/IVHmay predict less severe disorderssuch DCD (Paneth, Pinto-Martin,1991)

1. Tertiary intervention studies withclumsy children have beeninfrequent

2. Such studies have not producedconsistent findings with regard tothe efficacy of partlicular approach(Miyahara, 1996))

DCD: Developmental Coordination Disorder; GM/IVH: germinal matrix/intraventricular haemorrhage

18 BRIAN HOPKINS

There are three common denominators withregard to each of these aspects of the clinicalcontinuum. To begin with, they all require theintegration of a variety of sources of information(for example, biochemical assays, brain scans,physiological measures, assessments of elicitedresponses, and evaluations of spontaneousmovements). The relative clinical significanceassigned to the various sources remains a problem.Another commonly shared issue is what constitutes’normality’. According to Feinstein (1977), theterm normality can have two general meanings:isolated and correlated normality. Isolatednormality is the same as ’normality as average’and as such depends on normative age standardsderived from standardized (developmental) tests.Correlated normality involves relating scores on a

broadly-based test (for example, the MovementABC) to some other variable that measures a

specific function (for example, reading ability). Itappears that research on clumsiness is becomingincreasingly reliant on this latter approach as ameans of identifying subtypes of children initiallyclassified as DCD according to the strictures ofsome predefined notion of isolated normality. Afinal consideration that permeates the clinicalcontinuum concerns its starting point: an

instrument of early detection should ensure thatthe rates of false positives and false negatives are

as low as possible, with perhaps the latter beingthe crucial benchmark as to its discriminativevalidity. If not, then diagnosis and possiblysubsequent steps along the clinical continuumcould be jeopardized.

Returning to Fig. 1, notice that early detectionhas been depicted as resting on two distinct methodsof evaluation: one derived from qualitative (orcategorical) assessments and the other fromquantitative (or dimensional) assessments. In termsof research on childhood clumsiness, quantitativedata is delivered, for example, by the MovementABC, whereas Touwen’s (1979) neurological

examination represents a qualitative form ofassessment. What are the respective roles of thesetwo methods, particularly in the context of earlydetection?

C. QUALITATIVE VERSUS QUANTITATIVEMETHODS

The qualitative assessments of, for example,the spontaneous general movements of younginfants is epitomized in the ground-breaking workof Hadders-Algra and her co-workers (for example,see Hadders-Algra et al., 1997), as well as that ofPrechtl and colleagues (for example, see Prechtl etal., 1997). Based on judgments about the qualitywith which such movements are expressed, thismethod of direct observation is not overly time-consuming, simple to use and more readily matchesclinical practice with its propensity for regardingdisorders as qualitatively distinct entities relativeto quantitative assessments. For its properapplication, however, qualitative assessmentrequires extensive clinical experience and clearstandards of what composes the normal range ofage-specific behavior. Without such requirements"...qualitative assessments run the danger ofproducing arbitrary and artifactual boundaries inseparating ’normal’ form ’abnormal’ and thecreation of catch-call categories to cover anyuncertainties between these two extreme

judgements" (Hopkins, 2002, p. 307).For their part, quantitative assessments (for

example, stemming from kinematic analyses oflimb movements) can help to address theseproblems. At the same time, such assessments can

enable the underlying pathology in controlmechanisms to be specified more precisely (seeSee. F). This benefit, when allied with a

qualitative method of assessment, can be found in

research on the gait patterns of children with

cerebral palsy (Gage, 1991). Thus, in general,


early detection, as well as diagnosis, prognosis, andtreatment evaluation, will be improved through theblending of repeated qualitative and quantitativeassessments. In conjunction with serial brainimaging, they serve as complementary sources ofinformation, each with their own strengths andweaknesses, from which clinical decisions can bemade. Such decisions should also profit fromtaking account of the age-specific dependenciesbetween perception, movement, and posture. Thissuggestion is particularly apposite for the practiceof early detection.

D. EARLY DETECTION: TAKING ACCOUNT OFPERCEPTION, MOVEMENT, AND POSTURE

The departure point for this topic is thecerebellum of the electrical fish Gnathonemuspetersii (Bell & Szabo, 1986). Despite the greatsize of its cerebellum, giving it a brain/weight ratio

greater than a human adult, this moromyriad doesnot possess outstanding motor abilities. What itdoes have is a highly refined sensory system inwhich the cerebellum, together with midbrain

homologues of the colliculli, plays a crucial role in

detecting sense information from electroreceptors.Thus, the cerebellum in this fish is a sensory ratherthan just a motor organ as with echolocating batsand cetaceans who also have hypertrophiedcerebella.

The point of mentioning this intriguing fish is

that labeling brain systems as either motor or

sensory may prove to be a fallacious exercise

because they can be both. More generally, and at

another level, (Gibson, 1975) posited somethingsimilar when referring to the inseparability of

perception and action. In his view, there is a

circular causality between them such that actions

constrain or enhance what is perceived and what is

perceived constrains or guides actions. Actions

themselves, however, are composed of task-

specific movements. Consequently, developmentconsists of changes in perception (for example,binocular vision that becomes adult-like at about 4months) leading to changes in movementssubserving a particular action relative to a specifictask (for example, reaching for and grasping a

suspended object) and vice versa (for example, theability to crawl creates new forms of perceptualexperience).

What is lacking in this scenario is reference toa mutual dependency existing between movementand posture. This dependency can be depicted asfollows: posture imposes constraints on the sortsof movements that are possible while movementsconstrain the organization of posture (see Fig. 2).

Extending the scenario in this way portrays thedevelopment of action as resulting from changes inthe task-specific couplings between perception,movement, and posture such that a change in one

component will give rise to changes in the othertwo. For example, a transformation from a body-centered to a spatially-oriented posture typically

IRCEFIION

ACI’ION

Fig. 2: Perception, movement and posture depicted as

the components of the perception-actionapproach to development. According to this

approach, developmental transformations in

action are the result of changes in the task-

specific couplings between the components.

20 BRIAN HOPKINS

occurring at around 3 months of age (Geerdink etal., 1994) will propagate change in the sorts ofmovements that are possible. In turn, these newmovements will alter what the infant is capable ofperceiving. Furthermore, change might also beinduced by alterations in the nature of the task.

Task-induced changes in the movements ofyoung infants is well exemplified in the work ofvander Fits and colleagues (1990a; 1990b). In one study(1999a), they showed that healthy fullterm (FT)infants even as young as 3 months could adjust their

postural muscles during goal-directed movements toaccount for variations in position in space (viz.supine, sitting semi-reclined, sitting upright). Inanother study, they found that relatively healthypreterm (PT) infants followed up from 4 to 8months of corrected age were unable to make suchtask-specific adjustments due to a high amount ofpostural activity across all three positions in space(1999b). This difference between FT and PT infantsis open to interpretation with recourse to the notionof motor equivalence (namely, a variety of differentmuscle contractions and joint rotations can berecruited to produce the same outcome). Thus, whattypifies normal development is the ability to modifyposture so that actions are appropriate to thedemands of a particular task. In contrast, infants atrisk for one or other developmental disorder such asDCD may lack this ability arising from an

inadequate sensitivity to external perturbations thataccompany positional changes in space.Consequently, facilitating postural control can

enhance the performance of goal-directed move-

ments in such infantsa topic that is addressed inthe next section by means of an example from arecent study.

E. EXAMPLE 1: POSTURE AND REACHING

In this study, 6-month-old infants who couldnot sit alone performed reaching movements when

seated upright in a modified chair and confrontedwith a small object in the body midline (Hopkins& RSnnqvist, 2002). The modifications providedsupport for the long muscles of the back, the hipsand upper legs as well as inducing extension of thespinal column (see Fig. 3).

High-speed, 3D video recordings were madeof their arm and head movements when seated inthe modified chair. The resultant kinematics werecompared with those obtained with the infantsitting in an unmodified chair. Among otherthings, it was found that reaching was smoother(contained fewer movement units) when theinfants were in the modified chair, but more so forthe right than left arm (see Fig. 4). In addition, thehead was more stable during reaching in thiscondition.

This study has potential implications for bothearly detection and intervention. For example,subjecting PT infants to seating modifications thatprovide additional postural support may help to

distinguish those really at risk for disordereddevelopment from those who are less likely tomanifest subsequent impairments or disabilities

Fig, 3: Modifications made to a commercially producedinfant chair: back rest 90 degrees to the sittingsurface (A), a sacral pad (B), a raised ledge on

which the infant sits (C), wells into which the

upper legs are inserted (D), and wedges placedagainst the hips (E).


(namely, compromised infants may show aninability to adjust their posture to such modifi-cations and thus any beneficial effects for theiractions). In terms of (tertiary) intervention, seatingdesigns for promoting postural control andmovements of the upper extremities in childrendiagnosed as being cerebral palsied have a longhistory of use in the practice of physical therapy(see Mulcahy & Poutney, 1986; Reid, 1996). Sofar, the benefits of these designs for such childrenamount to only promising claims, perhaps becauseof a lack of evaluations using appropriate controlsand more objective measures.

At least, the kinematic parameters that wereincorporated into the present study might contributeto improving the scientific rigor with which theseevaluations are conducted. In the next section, we

RIGHT LEFT BILATERAL

Fig. 4: Mean number of movement units (MUs)contained in unilateral (right or left arm) and

bilateral reaches made when infants seated in

unmodified (o) and modified (o)chair. Overall,there were significantly fewer MUs for reaches in

the modified chair [F(1,207)= 11.30, p<.001].More specifically, there were significantly less

MUs during unilateral right and bilateral

reaching movements compared to unilateral left

arm reaches in this condition.

shift from quantitative assessments of reaching totheir use in kinematic registrations of spontaneousleg movements performed by healthy infants andthose with a verified brain lesion. What differencesin performance do they detect between the twogroups of infants?

Fo EXAMPLE 2" PERIVENTRICULAR LEUKO-MALACIA AND KICKING MOVEMENTS

Periventricular leukomalacia (PVL) consists ofbilateral necrosis in the periventricular whitematter, which leads to the formation of cysticlesions at the comers of the lateral ventricles in thefrontal, in the parietal, and less often, in theoccipital regions. Present in about 9.2% of verypreterm (VPT) infants but varying according to

gestational age (Zupan et al., 1996), the causes ofPVL are a matter of debate. Nevertheless, onelong-term outcome is indisputable: in most VPTinfants, PVL is associated with spastic diplegia(Volpe, 1995). Less severe forms of PVL havebeen implicated in the etiology of clumsiness(Hadders-Algra, in press) and related conditionslike the Nonverbal Learning Disabilities Syndrome(Rourke, 1995).

In a study of PT infants with PVL verified byMRI, 3-D movement registrations were made oftheir spontaneous kicking movements in supineand compared with those of healthy FT infants atthe (corrected) ages of 6, 12, 18, and 26 weeks(Vaal et al., 2000). For those PT infants with theseverest forms of PVL, the cross-correlationsbetween the three joints of the (right) leg duringkicking became increasingly higher over agecompared with their healthy counterparts who hadmarked decreases in values after 12 weeks (seeFig. 5 for hip-knee cross-correlations).

Each infant with severe PVL had extensive

damage to the corticospinal tracts, which suggeststhat they are involved in the regulation of intralimb

22 BRIAN HOPKINS

Fig. 5: Mean hip-knee correlations, converted to Z-scores,obtained longitudinally for healthy fullterm infants

(o) and those with periventricular leukomalacia (o)during spontaneous kicking at the (corrected) agesof 6, 12, 18 and 26 weeks. Excluded from this figureare those infants with mildly and moderatelyabnormal indications of periventricular leuko-malacia. Similar age-related trends were found forthe hip-ankle and knee-ankle cross-correlations

(see Vaal et al., 2000).

joint dissociations between 4 to 6 months of age.These tracts do not appear to play a direct role ininterlimb coordination as there were no groupdifferences across age in the relative frequency ofsimultaneous and altemating kicking movements.To investigate the possibility that the coordinationbetween leg movements is not regulated directly bythe corticospinal tracts, a subsequent study wascarried out (Vaal et al., 2002). Now, small weightswere applied to the right leg of PT infants withPVL and their healthy FT counter-parts at 26weeks corrected age (the age at which infants withand without PVL differed most in terms ofintralimb coordination as revealed in the previousstudy).

In short, there were no differences in therelative frequency of altemating and simultaneouskicking between the two groups of infants anoutcome lending further support to the contentionthat cortical centers are not involved in theregulation of interlimb coordination. The PVLinfants, however, increased their overall rate ofkicking in the weighted condition relative tobaseline (without weighting), which was not thecase for the FT group.

The latter finding not only implicates thecorticospinal system in adjusting the combinedkicking frequency of both legs to an externalperturbation but also says something about thecoupling between proprioception and movement inhealthy and in brain-damaged infants. Onepossibility is that the former galvanized functionalsynergies in such a way that they did not have toincrease kicking frequency when the leg wasweighted. In contrast, the PVL infants ’over-reacted’ to weighting the leg as shown byincreases in the frequency of kicking compared tobaseline. This difference implies perhaps that thehealthy developing nervous system can increasinglyexert a feedforward control over proprioception,whereas one compromised by cortical damagereacts in a feedback mode, at least with regard to

leg movements. The ability to use a feedforwardmode of control, perhaps by means of adjustingmuscle torques to produce similar amounts ofkicking in the weighted and baseline conditions, is

probably achieved sooner than 6 months after birth

(see Schneider et al., 1990). Representing another’example of motor equivalence, this and otherfindings in the study also stress quantitative(kinematic) assessments as a useful adjunct to

methods of early detection.Returning to the point that the corticospinal

tracts do not seem to play a major role in interlimbcoordination, an altemative possibility in this

respect could be the mesencephalic locomotorregion (MLR). Electrical stimulation of this


circumscribed region of the brain stem induces anormal pattern of walking in decerebrate cats on atreadmill (Shik & Orlovsky, 1976). Similar findingshave been reported for the neonatal rat (Atsuta etal., 1990), which suggests that this monoarminergicsupraspinal descending pathway involved in thecontrol of spinal rhythm generators is functional atbirth. In infants with cortical PVL, the MLR ismost probably not damaged, thus enabling them tocoordinate movements of the legs in ways that are

indistinguishable from healthy controls. Thissuggestion, however, has two caveats. First, otherbrain stem structures like the subthalamic locomotorregion and the pontine locomotor region (viz., thependunculopontine nucleus) can generate walkingmovements when stimulated (Armstrong, 1988).At present, how they and the MLR interact in thecontrol of normal locomotion is unknown. Second,and most important, it still has to be demonstratedthat these locomotor regions have homologs in thehuman.

Go CONCLUDING REMARKS: BACK TO THECLINICAL CONTINUUM

The main argument in this paper has been that a

greater understanding of the links betweenperception, movement, and posture in thedevelopment of action can engender furtherimprovements in the instruments of early detection,as well as in other aspects of the clinical continuum.As part of this theoretically-driven venture,attempts should be made to test the functionalintegrity of the young nervous system through’tweaking’ it with the appropriate experimentalmanipulations (for example, by means of variationsin spatial position, load, and other mechanicalperturbations). But when should such ’tweaking’take place? One suggestion rests on theassumption that the susceptibility to task-induced

changes in action could be particularly marked

during transitional periods in development whenthere is a heightened sensitivity to externalperturbations (see Hopkins et al., 1993). Duringthese periods, which can be empirically verified

(see Hopkins, 2001), infants whose nervoussystems have been adversely affected in some waymay display an inability to achieve motor

equivalence across variations in experimentalconditions. In other words, they evince a lack offunctional plasticity. Such children might, of course,take longer to achieve a particular transition oreven not make it all.

Moving to the other end of the clinicalcontinuum, timing should also be a considerationas to when primary or secondary intervention ismost appropriate. More to the point, the questionis how early it should be applied? One answer(Hopkins, 2002) stems from the concept ofontogenetic adaptations (Oppenheim, 1981)" certainstructures and functions are needed for survivalduring one period of development, but they may beunnecessary (or even detrimental) for adaptationsat later ages. Consequently, these structures andfunctions must be eliminated, suppressed, or

reorganized in the course of normal development.At the functional level, such a major change inhuman development resulting in better adaptationto the extrauterine environment is evident some 2to 3 months after birth (Prechtl, 1984). Thus,therapeutic intervention before about 3 monthscould create iatrogenic effects, due to it sustainingprenatal adaptations that would otherwise disappearabout this age in normal development. This viewdoes not run counter to current medical practicewith regard to preterm infants, some of which isdirected towards catering for their poor activepostural control. Rather, this notion warns againstthe penchant for ’intervention as early as possible’that is typical of some advocates for programs ofsensory stimulation with such infants.

As a final point, a testable theory embracingall aspects of the clinical continuum is lacking.

24 BRIAN HOPKINS

Without new theoretical impulses, the practice ofearly detection and the rest will only stagnate. Onesuggested impulse derives from Edelman’s (1987)Neuronal Group Selection Theory (Hadders-Algra,2000). This theoretical perspective is in manyways consonant with the perception-action approachto development, all too briefly outlined in thepresent paper. Together, they could provide animpetus for us to integrate each aspect of theclinical continuum into an all encompassing theorythat is applicable to research on developmentaldisorders. Such would be particularly beneficialfor future studies on children who are afflictedwith clumsy behavior, given that in the past therehas been a paucity of theorizing about how thetriad of perception, movement, and posture co-

develop in such children.

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