neuropsychological identification of motor problems: can we learn something from the feet and legs...

Neuropsychology Review, Vol. 1, No. 2, 1990

Neuropsychologicai Identification of Motor Problems:

Can We Learn Something from the Feet and Legs That Hands and Arms Will Not Tell Us?

M i c h a e l P e t e r s 1

The degree of structural and functional specialization that differentiates between upper and lower limb use in humans is quite unparalleled among primates. It is argued that less neural resources are devoted to leg and foot control than to arm and hand control, and that this aspect o f lower limb innervation, together with the uniquely restricted use of the lower limb, renders lower limb function more sensitive to general neural insult. In addition, the status of leg and foot control differs from that of arm and hand control both early in life and during the later years o f decline.

KEY WORDS: foot arid leg neuropsychology tests.

INTRODUCTION

This paper deals with abnormal and normal movement of the legs and feet within a general context of human movement. No attempt is made to review the literature on upper or lower limb control as such. The intent of the paper is not to interpret or explain different aspects of upper and lower limb function, but to raise the possibility that the status of lower limb motor control may under some circumstances be a more sensitive and informative measure of maturational and functional status of the motor system than the status of upper limb motor control.

A previous paper dealt largely with asymmetry in foot performance and skill, and touched upon the value of assessing foot movement for neuropsychological purposes (Peters, 1988). This latter aspect will be fully developed here. The following relevant aspects will be considered: (1) comparison of up-

~Department of Psychology, University of Guelph, Guelph, Ontario, Canada NIG 2Wt, 165

1040-7308/90/0600-0165506.00/0 © 1990 Plenum Publishing Corporation

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per and lower limb use; (2) Implications for neuropsychology-(a) unclear pathology and developmental retardation, and (b) established pathology in lower limb function; and (3) what to measure.

COMPARISON OF UPPER AND LOWER LIMB USE

Humans Show a Greater Degree of Functional and Structural Differentiation Between Arms and Legs Than Other Primates

The justification for dealing with lower limb movement in isolation stems from the unique status of the lower limbs in humans as opposed to subhuman primates. In the latter, the lower limbs are not as exclusively dedi- cated to locomotion as they are in humans (Buettner-Janusch, 1966) and do not as a result show the same degree of functional and structural specialization. The feet of subhuman primates are extensively used for grasping in brachiation and manipulation, and are less distinct in their adaptation from the hands than is the case for humans. If humans retain some manipulative ability in the feet it is not because of the development of new abilities but because of the retention of phylogenetically older abilities.

No Evidence for Qualitative Differences in the Neural Control of Arms and Legs, But It Is Difficult to Generalize Subhuman Primate Data to Humans

The first question to be asked is whether the distinct contrast between upper and lower limbs in the human implies a qualitative diference in sensory motor relations between the two sets of limbs. In several studies Brunia and colleagues (e.g., Brunia et al., 1985) have shown that while movement- related potentials for manipulation of the fingers are seen primarily in the cortex contralateral to the moving hand, such potentials are predominant in cortex ipsilateral to the moving foot. Does this suggest a fundamental difference between the motor innervation of upper and lower limbs? Boschert et al. (1983), and Boschert and Deecke (1986), point out that the area in which foot movements are represented is located close to the midline and the di- pole actually points toward the other hemisphere, an interpretation that was first advanced by Brunia (1980). Both the fact of ipsilateral predoininance and differences in polarity of the initial phases of the registered potentials are explained in terms of the anatomical differences in location of hand and foot areas in the primary motor cortex.

Clinical information is quite clear on the basic contralateral innervation of both the hands and feet, as illustrated by Brodal (1973), who described

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that both finger extension and foot dorsiflexion on the left side were abolished after a stroke in the right cerebral hemisphere. The work of Lewis and Brind- ley (1965) suggests that the difficulty with extensor responses is likely due to pyramidal tract lesions. In spite of these functional similarities, there are some anatomical differences with regard to the pyramidal tract. Some 50% of the pyramidal tract fibers end in the cervical region, with a further 20% ending in the thoracic region, leaving only some 30°70 to end in the lum- bosacral region (Lassek, 1954). It is also quite likely that other anatomical differences exist. For instance, in tracing callosal fibers connecting the sensory and motor cortices in primates, it is found that relatively few transcal- losal connections exist between the primary motor and sensory areas for the hand. In primates, the same can also be said for the feet (Cusick and Kaas, 1986). This paucity of connections has been related to the need for indepen- dence when the hands perform different movements toward a common goal. In subhuman primates, it is reasonable to expect that the same principle holds for the feet. In humans however, where the feet and legs are specialized to perform a far narrower range of activities than in subhuman primates, the expectation of a lack of crosscallosal fibers connecting the foot regions is not nearly as strong. No anatomical information is available on this point.

In drawing on data from neuroanatomy and neurophysiology that per- tains to foot function, it is important to keep in mind that much of what we know derives from subhuman primates. While it is likely that information gained about the circuits controlling the hands of such animals is quite relevant to the human condition, the fact that the lower limbs of subhuman primates are not nearly as specialized as those of man suggests that the information gained about functional and structural parameters of lower limb motor control is not as clearly relevant to the human condition. One indica- tion of the different status of the lower limbs for humans and subhuman primates is the claim that pyramidal tract lesions tend to affect the lower limbs of monkeys more severely than the upper limbs (Patton and Amassi- an, 1960) while the opposite is true for humans (Elliott, 1963). The explana- tion for this difference is perhaps to be found in the somewhat reduced role played by the pyramidal innervation of the lower limbs in the human.

Hand Movement in Skilled Manipulative Tasks is Relatively Less Integrated with Postural Control Mechanisms Than is the Case

for Foot Movement

It is quite true that practically all voluntary movements that involve arm and leg use have to be integrated with postural control mechanisms. Nevertheless, the upright stance in the human has different implications for

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the immediacy with which arm and leg movements relate to postural control. In case of manipulative movements of the hands, movement can be largely freed from a need to be integrated with postural control mechanisms unless the movements require such integration. In contrast, there is little that is done with the feet and legs by way of skilled and manipulative movement that does not demand a delicate integration with postural control. The complex interlacing of voluntary with automated postural control in case of the feet requires extraordinary means for fast disconnection from postural control if such is needed for voluntary movements. There is some reason to believe the large and fast fibers that extend from the Betz cells of the motor cortex to the spinal cord, of which the very large majority project to the lower spinal cord, are involved in such disconnection (Horanyi, 1958).

The Focus of Attention on Upper and Lower Limbs Differs in the Performance o f Skilled Tasks

An important distinction between upper and lower limb function in humans is the somewhat reversed relationship between feet and legs and arms and hands. While the hands constitute a focus of attention in many normally occurring skilled activit ies-with arms forming an essential but not directly attended to element, the reverse can be said for the majority of skilled leg movements. In the latter case, it is the leg movement as a whole that receives attention and the feet are not normally receiving separate attention. This, at any rate, is part of the argument that independent control over the distal port ion of the legs is not normally as developed as that in the distal portion of the arms; the relative size of the cortical sensory and motor representa- tion of the hand and feet areas supports the distinction. Nevertheless, it would be a mistake to ignore evidence of considerable plasticity in the motor systems serving the lower leg. The most impressive evidence comes from persons who were born without functional arms or hands. In such cases there may be a considerable rearrangement of motor pathways. In the remarkable book Learned Pigs and Fireproof Women, Jay (1987) documents a number of relevant case histories. Of these, the ones that involve the playing of musical instruments are perhaps most relevant because such activities are the clearest evidence of delicate independent toe control in manipulation. Pietro Stadelman, an Italian, played the dulcimer with his feet, and Jean de Hanau, a Frenchman, gave mandolin concerts in likewise fashion. Most remarka- bly, Carl Herman Unthan, about whom extensive documentation exists, mastered the violin with sufficient skill to be allowed to play on Paganini's Stradivarius. Unthan also was a skilled typist with his feet. Perhaps equally remarkable, an armless Japanese woman, Madame Hanakawa, impressed

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her contemporaries with her accomplished origami paper folding art. These examples suffice to point out that skilled independent use of the lower extremities is possible and can, even though this is not normally the case, reach remarkable levels of accomplishment. Whether or not this is done with a neural circuitry that is comparable to that found in the average person or whether extensive rerouting of pyramidal tract fibers very early in development takes place is, of course, not known.

IMPLICATIONS FOR NEUROPSYCHOLOGY

Having outlined some of the maj or differences and similarities between hand and foot specialization, foot movement will be considered within the general context of normal vs. abnormal function. The reason for singling out foot movement is based on the hypothesis that the unique demands placed on the feet and legs in the human lower limb render control vulnerable to a variety of insults. The primary objective of the focusing of attention on foot and leg movement does not, therefore, consist of an attempt to deal with foot and leg movement as such, but as an indicator of general problems with the central nervous system. In the following, a distinction is made between clearly established pathology and cases where pathology is not clearly established, or not well understood. The latter aspect will be discussed first.

Unclear Pathology and Developmental Retardation-Developmental Aspects

One of the indicators that motor control of the lower limbs in the human has an unusual status comes from the observation that control of simple locomotion lags behind control of the hands. The difference in the maturation of the systems underlying locomotion and manual skill is most clearly seen in the performing arts. While precocious musical talent finds remarkable expression in instrumental performance, an equivalent precocious- ness in motor control in dance is unknown. This is not surprising because even the development of a normal adult walking pattern is seen only at about 5-6 years of age in normal children (Berger et al., 1984). Because mastery of the lower limbs takes a long time in children who develop normally, this aspect of motor maturation is of great interest in the context of retarded development as well, and delay in motor milestones is given a prominent role in the assessment of mental retardation early in life. As an illustration, the average age at which Down's syndrome children manage to build a block of 2-inch cubes is 20 months, while the average age for normal control children is 14 months. However, the average age at which Down's syndrome chil-

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dren walk up a set of stairs while being helped is 30 months while the equivalent figure for normal children is 17 months (Cunningham, 1982). Two aspects are noteworthy. First, that it takes quite a bit longer for normal children to walk up a set of stairs with help than to perform the relatively complex task of building a tower with cubes, and second, that the gap between the two groups in the task involving leg use is both relatively and absolutely larger than in the task involving the use of arms. It should be noted that while normal children can, with assistance, walk down a set of stairs at about the same age as walking up, Down's children take another average six months before they walk down a set of stairs. Because there is the possibility that Down's syndrome children have specific cerebellar problems (Gibson, 1978) that affect the legs more than the arms, this comparison may perhaps be unreasonable. However, it does illustrate why in the assessment of retardation delayed motor milestones are of great interest, and why disturbances in gait and posture are of diagnostic interest in this context.

If mastery of the use of the legs is slow to develop in childhood, then it is not unreasonable to assume that the integrity of gait is sensitive to disturbances in old age. Such is the case (Woollacott, 1986). It appears that there are multiple causes for the deterioration of gait in the aged, but a marked reduction in the hair cells in the vestibular system (Rosenhall and Rubin, 1975) with age and a loss of lower limb receptors that are important in controlling posture (Whanger and Wang, 1974) are likely important factors.

Clumsiness in Leg Movement

Having established that the upright mode of walking demands much of the central nervous system, requires a long time to master, and is sensitive to any losses of efficiency in the controlling systems, the question of how this relates to suspected abnormality needs to be addressed. We begin with a concept useful in description of motor difficulties and controversial as to diagnostic usefulness. This concept is "clumsiness." Ironically, in every- day life, clumsiness is often used in the context not of the process of movement but of the outcome. For instance, a person who knocks over a glass of wine with an impulsive (but motorically perfectly executed) motion ex- cuses him or herself for being clumsy. However, we will adopt here the liter- al meaning of clumsiness: does not move well.

This hardly seems a basis for classification. However an analogy to mental retardation, where similar use is made of "does not think well," points out that there is something of value in this concept. In mental retardation, it is customary to distinguish between people who are retarded because of organic causes and people who are retarded because they represent the low end of the normal distribution. Customarily, the lower end of the normal

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distribution is fixed in the IQ range of somewhere between 50 and 70 (Zigler and Hodapp, 1986), with persons having an IQ above 70 being considered of low normal intelligence while persons with IQs below 50 are considered retarded due to organic causes. However, there are those who believe the numerically large proportion of people with IQs between 50 and 70 are to be included in the organic category as well (Richardson, 1981). The underlying idea is that organic causes are present but have simply not been identified in these cases. That view was considered unorthodox for some time, but begins to be more plausible with the recognition of the fetal alcohol syndrome and the fragile X syndrome. The aspect that is of interest here is that at a certain point of the normal curve, intelligence may simply not be sufficient to convey an adequate selective advantage in the struggle for survival and is therefore not within the range of normal variation.

By analogy, it may be suggested that in the admittedly broad range of individual motor skill there comes a point where coordination and speed is lacking to such an extent that it would not, in our evolutionary past, have been sufficient for adequate individual survival and effective competition for procreation. By implication, the idea is that clumsiness is not a normal condition and that an organic component underlies clumsiness. The statement by Dare and Gordon (1970) that "Children are not by nature clumsy and, once the toddler stage is passed, the grace of movement of the average child is something to be admired" (p. 178) may be considered appropriate in this context. There is another implication of Dare and Gordon's observation that relates directly to the question of what is normal and what is not normal in movement: a lack of grace is noted immediately. Indeed, as spe- cies we share with subhuman primates an extraordinary ability to "read" movements in conspecifics (Peters and Ploog, 1973). The rather narrow band- width that humans are willing to accept as normal movement has been remarked upon in a broader context by Gahagan (1975). However, the ability to detect minor aberrations in movement is not based on an analytic ap- praisal. For instance, we can label a person as having a peculiar walk but will have difficulties in identifying cues that allow us to make that statement in an objective way or in backing up the observation by measurement. Our ability to identify as abnormal certain patterns in gait and posture leads to common inferences. For instance, it is rare that mentally retarded persons move with a normal degree of grace. Illingworth (1968) and Dare and Gor- don (1970) comment on the difficulty this creates for clumsy children because often an inference on their mental status is drawn on the basis of how they move.

Henderson and Hall (1982) found in their investigation of clumsy children that the simple test of how long children could balance on one leg without being able to make compensatory movements with the arms discriminated

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their group of clumsy children as well or better f rom control children than tests of complex manual skill. This finding is not unique. Many studies of clumsiness have identified measures of lower limb control as effective discrim- inators (Dare and Gordon, 1970; Gubbay, 1978; Gubbay et al., 1965; Hulme et al., 1983; Illingworth, 1968; Lesny, 1980; Shaw et al., 1982; Reuben and Bakwin, 1968). These studies, and many others of a similar nature, indicate that clumsiness in lower limb movement is rather often seen in the child la- beled as clumsy. Problems in lower limb control may be more enduring than other problems, as a case report f rom Illingworth (1968) illustrates:

I found motor development delayed, a normal intelligence, and no other abnormal physical signs. At 22 months she was first able to stand, holding on to objects; at 23 months she could sit without support; at 25 months she could walk, holding on to the furniture; and not until 50 months did she walk without help. But at the age of eight years her I.Q. score was 118 and she was doing well at school, playing games normally, though described as not being nimble on her feet. (p. 540)

The argument made in this section is that in the exploration of clumsiness, a closer examination of lower limb function is worthwhile. At present it is not clear whether developmental clumsiness can exist separately in upper or lower limb movement or if the most common underlying causes of clumsiness simply make lower limb movement more vulnerable. Research intended to answer these questions is bound to be fruitful both on the applied and theoretical level.

Established Pathology in Lower Limb Function

In this section, lower limb function will be discussed with explicit reference to pathology. In many disorders involving movement , both the upper and the lower extremities are affected and a categorical separation is point- less. In some cases a dissociation of the effects on upper and lower limbs can be observed but is essentially due to trivial factors, such as differential effects on a rm and leg movement by differently localized lesions in the pyramidal motor system. In such cases it is possible to explain the different severity in terms of the different ways in which the pyramidal system inner- vates proximal and distal parts o f the upper and lower limbs. However, it should be noted that while testing of the digits o f the hands in pyramidal motor system disease is generally carried out in some detail, the assessment of leg movement is usually restricted to locomotion and a limited range of skilled movements. Closer examination of residual motor function after strokes, tumors, and head injury might reveal nontrivial differences in the

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degree to which hand and foot movement is affected by the brain damage. Such a nontrivial difference, all things being equal, might be the relatively more severe effect of pyramidal tract lesions on the upper limbs in humans and the lower limbs in subhuman primates (Elliott, 1963; Patton and Amas- sian, 1960).

Outside of the pyramidal system, there are numerous nontriviaI exam- pies of how a disturbance in the central nervous system is differentially expressed in the upper and lower limbs, and often the effects are more clearly visible in the lower than in the upper hmbs. The most prominent famiiy of such dissociations involves posture and gait when some aspect of vestibulo- motor integration is implicated. When the anterior cerebellum (spinocere- bellum) is damaged, either through lesions or through viral or toxic agents, the lower limbs are markedly affected, with relatively minor effects in the upper limbs. This region came first to attention when k was noted that the ataxia in gait seen in some chronic alcoholics could be related to degenerative changes of the anterior cerebellum (Lhermittee, 1935; Victor e ta l . , 1959). It was noted that in such cases the problems with gait and stance were relatively m o r e severe than problems with the upper limb. There is some reason to believe the problems that intoxicated persons have with walking in a straight line can be attributed to a temporary impairment of the anterior cerebeltar region as well (Dow and Moruzzi, 1958). It is of interest to note here the different effectiveness of various tests in identifying deficits in the chronic alcoholic. Matsuoka e t al., (1986) note that in body balance tests on 38 alcoholics, some 84.2°70 of the patients gave positive signs on the stepping test (with eyes closed). The Romberg test proved much less sensitive with either eyes open (7.9070) and eyes closed (23.7070).

In Friedreich's ataxia the first observable symptoms involve gait problems and this has been related to the disturbance of a proper input into the anterior cerebellum from the spinocerebettar tracts. It is quite possible that a fairly large range of clinical effects on lower limb control may" be attributed to anterior cerebellar function. For instance, the effects on lower limb control caused by acute intoxication with lithium or toxins introduced through tick bite are expressed via an anterior vermis syndrome (Matsuoka et al., 1986; Mongan, 1979). The commonly observed effect in animals hit with tranquilizer darts, that the hindlegs show an effect earlier and more strongly than the forelegs, is likely due to an anterior cerebellar effect as well. One of the possible reasons for the prominent role of cerebellar signs is the susceptibility of the cerebellar cortex to all manner of insults. Dow and Moruzzi (1958) note the sensitivity of the cerebellar cortex to a variety of agents, and suggest that the Purkinje cells are the most sensitive of all central nervous system cells to high body temperature, which would explain gait ataxia after heat stroke. To the extent that gait disturbabces are very

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sensitive to cerebellar damage, a good case could be made for the careful testing of gait after exposure to various toxic agents (including heavy me- tals, such as mercury and lead) that have an impact on cerebellar function.

Disturbances of gait cannot only be produced by way of cerebellar dysfunction but also by direct effects on the vestibular system proper. It is well known, for instance, that some aminoglycide antibiotics (e.g., streptomy- cin) have a direct effect on vestibular hair cells.

Abnormal foot and leg movements are also of interest with regard to the understanding of the apraxias, and the review by Brun (1921)- who was the first to describe leg apraxia in 1892-shows that earlier researchers had taken note of the phenomenon with regard to the lower limbs. Current at- tempts to classify apraxias are partly directed at identifying the level at which problems occur, e.g., at a level that is close to the formulation of motor plans or closer to the level of execution (Roy and Square, 1985). Connected with this question is the attempt to see if apraxias are specific to certain motor systems. For instance, Kimura (1982) would hold that the left hemisphere is involved in the sequencing of movement across systems, and that therefore apractic disturbance involving sequencing should be expressed in several motor systems. The literature on leg and foot movement apraxias is quite limited. Part of the reason for this is expressed by Poeck (1986), who states that in limb kinetic apraxia arms and legs are affected, and that legs do not need to be tested separately because no additional information can be expected. Poeck also suggests that tests for ideomotor apraxia are limited to the upper limbs because there are no good tests for the lower limbs and dissociation is rare. The neglect of the legs in apraxia testing is common. In the interesting case of an apraxia after basal ganglia and thalamic damage, De Renzi et al. (1986) mention leg involvement but no specific testing of the legs. A brief glance at tests for apraxia as given by Brown (1972) shows that tests for apraxia in leg function are indeed limited (stamp out cigarette, press on gas pedal, tap foot, kick a ball, slide foot in slipper). There is a question (Brown, 1972) of whether there is such a thing as gait apraxia, where the disturbances are attributed not to a primary problem in the execution but in the organization of leg movements during walking. Brown concludes that gait apraxia can be attributed to a lack of strength, motor initiative, and coordination problems, and should therefore not be considered a true form of apraxia. Denny-Brown (1958) suggests that the causal factor in the gait apraxia observed after frontal lesions is an exaggerated grasp response of the toes that interferes with normal placing. If one takes as defining criterion for gait apraxia the lack of any obvious impediments to the execution of walking movements, Denny-Brown's frontal gait apraxia does not quali- fy as a case of true apraxia. Meyer and Barron (1960) showed, however, that gait apraxia after frontal lesions can be seen in the absence of a persistent

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foot grasp response. Meyer and Barron (1960) felt the primary difficulty in gait apraxia was a difficulty in movement initiation. Unlike Brown (1972), they did not consider this particular etiology as precluding the classification of gait apraxia as true apraxia. Meyer and Barron, as others, addressed the question of whether frontal gait apraxia could be considered a purely frontal syndrome or whether is was due to disruptions of frontocerebellar connections. The prominent effects of cerebellar damage on gait have previously been described. Meyer and Barron suggested that gait apraxia specifically due to frontal damage can be differentiated from cerebellar effects. In particular, in the former case there is a slowness in the initiation of movement, a tendency to deviate in the direction of the affected leg in performing the "star-gait" test, and most notably, difficulties in describing an imaginary circle with the feet, tapping the heels on the floor, and kicking an imaginary ball. Case 5 of Petrovici (1968) had trouble initiating walking but could walk relatively welt once started, in support of Brown's interpretation. However, it is of interest to note that while this patient could describe a circle with both hands he was unable to do so with the feet. This patient could not kick an imaginary batt but could touch object on the floor on command. Both Cases 3 and 4, according to Petrovici, did not know what to do with their legs when asked to walk. Case 4 simply stepped in place when asked to walk and progressed only when pushed from behind. Meyer and Barron (1960) describe their Case 3 as having great difficulty in performing simple movements with the feet on command. This patient could perform coordinated movements slowly but correctly with the hands. Case 7 was perhaps most interesting as he could kick a real but not an imaginary ball. In none of the cases is there a suggestion of a dissociation of apraxic disturbances in upper and lower limbs, or that a unique and separate kind of gait apraxia exists. However, there is a possibility that the lower limbs might be more sensitive indicators of apractic disturbances than the upper limbs, and that more refined tests of leg and foot apraxia might be quite informative. The argument in favor of such a possibility is the same as was made above for other forms of upper/lower limb dissociations: Disturbances are more likely to show up in the lower limbs because there are generally fewer neural resources committed to the circuitry that permits voluntary use of lower limb movement. Through- out the literature on apraxia, there is an emphasis on problems in initiation of movement. In his classical review, Wilson (1908) comments on the term "Willenlosigkeit" (literally: will-lessness) that was used extensively in the Ger- man literature on apraxia. While Wilson did not make any mention of leg movement at all and referred to upper limb apraxia only, it is clear (Brown, 1972; Meyer and Barron, 1960) that difficulties in movement initiation are a very significant factor in gait apraxia as well. In contrast to this problem in initiating leg movement is the opposite problem, the "restless leg syndrome"

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(Montplaisier et al., 1985). Patients with this syndrome have a very strong urge to move their legs and walk, and while they can manage to contain the urge for some time they will eventually succumb and give in to the impulse.

In evaluating the clinical literature on gait apraxia it becomes clear that the term is often used in the presence of motor problems that might contrib- ute to difficulties in walking, and would therefore not be considered as a true apraxia. For instance, various recent reports mention gait apraxia in Rett's syndrome (Adkins, 1986; Brunel and Gilly, 1985; Estanot, 198t) and gait apraxia is considered a diagnostic criterion for Rett syndrome (Rett Syn- drome Diagnostic Criteria Work Group 1986), even though children with this syndrome have widespread motor problems. Similarly, in the literature on hydrocephalus, gait apraxia is frequently mentioned (Knutsson and Lying- Tunnell, 1985; Sudarsky and Simon, 1987), even though it is acknowledged that there are various underlying motor problems. In fact, Sudarsky and Si- mon (1987) feel gait problems in hydrocephalus patients are due to a sub- cortical motor control disorder and should not be classed under the category of apraxias. What is clear, however, is that measurement of gait in hydrocephalus is important and useful because it is a sensitive indicator that responds well to a reduction in intracranial pressure (Knutsson and Lying- Tunnell, 1985).

In senile dementia, both of the general and Alzheimer's type, gait apraxia can be observed (Barton, 1967; Horenstein, 1974; Kulczycki and Jedrzejc- zak, 1984) in the presence of relatively normal reflexes, and unless the dementia is of a reversible type, the prognosis for improvement is not good. In associating various abnormalities seen in Alzheimer's disease with the severity of the disease, however, only a mild association was found between general severity of the condition and general gait abnormalities (Huff and Growdon, 1986). The authors state that a strong association was found between the severity of the disease and aphasia and apraxia. To the extent that the presence of primitive reflexes was one of the factors associated with in- creased severity, it is once again not possible to dissociate the apractic condition from accompanying motor disorders that might affect execution of movement. At any rate, in Alzheimer's disease, apraxia of skilled leg movements might be found in the absence of a gait apraxia.

W H A T TO M E A S U R E

So much for the general sensitivity of lower limb movement to subtle and clearly defined pathology. Measurement of disturbances of lower limb


function is most often based on individual clinical experience and involves observation of a few common activities. The neurological screening proce- dures described by Klein and Mayer-Gross (1957) are representative of tests for lower limb dyspraxia. They suggest that the examiner evaluate walking, running, hopping, knocking with the heel on the floor, standing to attention, turning, describing a circle with each leg, and kicking a bail.

Unfortunately, there exists no comprehensive battery of lower limb function in the neuropsychological repertoire that provides standards for testing. Such standards have yet to be established. In the following, a prelimi- nary catalogue of some of the motor aspects that have to be assessed by lower limb tests is given.

Balance

Here, the vestibular control over posture is examined. This can first be done in terms of static balance, in a variety of levels of difficulty (one leg, with and without compensating arm movements, two, legs, one foot in front of the other, with degree of difficulty determined by the surface upon which the foot rests). Postural control can also be examined in terms of its integration with gait. Here, rate of walking and the nature of the line or raised surface to be walked upon is an important variable~ This type of test will examine the vestibular system proper, and in balanced gait the dimension of visual control can be included as well. It should be noted that while postural tests (e.g., Romberg test) are used in neurological applications, they tend to look for marked impairment and are generally not sensitive enough to examine mild impairment on the basis of deviation from established norms. Fregly (1974) notes that if the method of measurement is improved, insensi- tive tests such as the Romberg test can be improved considerably. Thus, while vestibular dysfunction in a person might not be identified via the Romberg test, a stabilometry platform could show impairment. In addition to a lack o f sensitivity, the specific purpose of clinical diagnostic tests usually has ted to a neglect in establishing norms, and such norms are needed in population screening tests. Some tests for posture and gait have been standardized for children; Stott et aL (1989) have provided norms for static balance on one and two feet, and dynamic balance for a walking task for children up to the age of 12. These tests are related to clinical tests for vestibular function, such as described by Fregly (1974). Further standardization work in this area is desirable.

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Manipulative Skill in the Lower Limbs and Reduced Influence of Postural Factors

Skilled activities in the feet such as are seen in kicking are inevitably contaminated with postural control. Thus, the lack of adequate performance can be due to problems in the latter or problems in motor control as such. Gardner (1941) has described numerous manipulative foot tests but these do not lend themselves to standardization. A test that is broadly used in exami- nations for clumsiness is a test that requires the sitting subject to dribble a ball around a number of objects on the floor (Hulme et al., 1983), but no standardized performance norms are available. Together with manipulative tests, tests of force production can be used (Carnahan et aL, 1986). In these, subjects are required to maintain a given amount of pressure on an object while sitting. Because such tests can show differences within one subject (one leg being better at the task than the other), it can be assumed that the sensitivity of force production tasks is great.

Foot Agility and Dexterity

One way of assessing this is by a speed tapping test, where subjects have to tap as quickly as they can. As is the case for finger tapping, foot tapping tests reveal a performance asymmetry, with the right foot generally tapping faster than the left foot (Augustyn and Peters, 1986; Malmo and Andrews, 1945; Peters and Durding, 1979). The foot tapping test might be seen as at- tractive because it appears to be one of the only tests where hand and foot performance can be compared directly. However, the general similarity of the task is deceptive. Peters and Durding (1979) could not identify a significant correlation between performance of the hands and feet on this task. This may be partly due to the somewhat artificial nature of this task for the feet, where a subject can tire very quickly. Another aspect is that while the capacity to perform rapid and precise movements of the individual hands represents the quintessential aspect of hand skill, such a capacity is perhaps less specifically selected for in the case of the feet. Nevertheless, as Malmo and Andrews (1945) have shown, the foot tapping test has the advantage of giving direct quantitative results. With regard to sensitivity, it is suggested that a test sensitive enough to identify lateral asymmetries will tend to have sufficient sensitivity in a clinical context.

Running Speed and Agility

It is true that running speed is a complex measure that not only involves the central nervous system but also the specific makeup of the muscles in


terms of the proportion of fast and slow twitch muscles. However, what was said about differentiating normal from abnormal degrees of clumsiness in general can also be said about running speed in particular: At a certain point, running speed will be so low that it cannot be considered part of the normal range of variability. In the absence of standardized data, a statement about what would constitute unusually slow running speed cannot be made. Be- cause of practical considerations, running speed in the testing context will not normally be measured in all-out running. However, an arguably adequate substitute (because some aspects of gait and postural control will be quite different) is running in place. A simple pressure plate arrangement could give quantitative information about stepping frequency. If room is available, an element of agility can be included by having subjects step rapidly from one target into another. Here, the agility training runs (stepping through a series of tires) used in football can readily be adapted. Standardization could be easily achieved.

Hopping and Jumping

Whether or not separate tests for hopping and jumping need to be developed is unclear. Hopping and jumping cannot develop adequately without good postural control and for this reason it is important to exclude vestibular/posturat factors when problems in this area are noted. Reuben and Bak- win (1986) report that on occasion a child may be unable to hop even though posture and gait seem intact. This suggests a dissociation, and perhaps a separate test that examines the ability to hop and jump may be appropriate. However, it is not at all clear if there is a categorical distinction between hopping and walking, or whether hopping simply represents a more demand- ing task for the neural circuitry by which leg movements are guided.

Integration of Leg Movement with Whole Body Movement

In the previous two categories, there must be an obvious integration of leg movement with whole body movement because effective locomotion or jumping in whatever context is quite unthinkable without such integration, Here, however, the focus is different in that the emphasis is not on the feet and legs, but oll other activities. The best illustration of such a category of tests is given by one of the tests in the Stott et aL Motor Test (1989, age band 3, dynamic balance 2), where subjects are to walk from one point to another while balancing a ball on a level board that is held in the hand. The subject is expected to focus on the primary task of balancing the ball on the board without dropping it while at the same time maintaining

180 Peters

locomotion. In order to be successful, the hand and foot movements have to be integrated very delicately. Such a test could be analyzed at various levels of sophistication; in the motor test alluded to, only the number of times on which the ball falls o f f the board is recorded. With a kinematic analysis, the nature of the errors can be captured and the way in which one activity has to yield to the other in case of a lack of integration can be documented.

The major categories of tests for foot and leg function outlined here are meant to provide sensitive indicators o f subtle impairments in the used of feet and legs, and are of use in screening and population applications where the nature and degree of motor impairment is expected to be subtle. All tests can be done simply or with varying degree of technical sophistication. For instance, vestibular tests of postural adjustment can attack the problem with help of platforms such as used by Nashner e t al. (1979). There is some question as to how specific such screening tests should be. That question can only be answered with reference to a factorial model of the guidance of leg and foot movement: How many different factors are needed to account fully for all dimensions of normal foot and leg movement?

S U MMA R Y

An argument is made that systematic testing of lower limb function should be part of exhaustive neuropsychological testing. While no attempt is made to suggest that qualitative differences exist between upper and lower limb motor control, it is suggested that the particular characteristics of struc- ture and function of the human lower limbs make their control relatively more sensitive to a variety of subtle and outright insults to the central nervous system. In the absence of fully developed and normed neuropsychological scales of lower limb movement, work toward the establishment of such scales will be of considerable applied and theoretical usefulness.

ACKNOWLEDGMENTS

This work was supported by Natural Sciences and Engineering Coun- cil of Canada Research Grant No. A 7054.

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