Manual Dyspraxia: A Lesson in Mind and Brain

Developmental K.

Ruthmary

Deuel, MD; Bertha

P. Doar

Abstract

decades, pediatricians assiduously documented "soft neurologic signs" in children referred for school learning difficulties, although pediatric neurologists, including Charles F. Barlow, pointed out the dissociation between most neuropsychological abnormalities and the motor findings in question. Later, large epidemiologic studies confirmed the For

independence of soft signs from other neuropsychological defects.

We used a standardized dyspraxia battery to study 164 schoolchildren 5 to 12 years old. We found that in the group as a whole there was a positive correlation between motor performance in the dyspraxia battery and IQ on the Wechsler Intelligence Scale for Children-revised (Full-Scale, Verbal, and Performance). In terms of dyspraxia subscales, we found that Performance IQ and Full-Scale IQ correlated with imitation of nonsense gestures and use of actual objects, whereas Verbal IQ correlated positively only with pantomime on command. In contrast, for the group of 24 subjects whose scores on the battery designated them as dyspraxic, there was no correlation between dyspraxia scores and IQ. Together with the existence of specific, dramatically different, types of dyspraxia among the 24 dyspraxic subjects, present findings uphold the earlier neurologic opinion that "motor soft signs" are not evidence for fixed "brain damage" or even for other types of motor dysfunction, and that dissociation of different JChild Neurol specific cognitive dysfunctions is the rule within individual patients. ( 1992;7:99-103).

oft neurologic signs, particularly

clumsiness have for decades created a great deal of confusion and even animosity among physicians, educators, and parents. &dquo;Soft signs&dquo; came to the attention of the general medical public in the 1940s together with the newly described neurobehavioral disorders of childhood, hyperactivity’ and autism.2 Margaret Kennard, a neurologist who early constructed a special examination for motor soft signs, explicitly defined them as findings on neurologic examination of either minimal intensity or findings that were present sometimes but not always.3 High frequency of such motor performance deficits has repeatedly been found in groups of children with attention and learning problems. 4-10 While recognizing the statistical association, neurologists were vehement in arguing against the tautologic reasoning that the presence of such signs

Sand

Received

dyspraxia,

August 8,

1991.

Accepted

for

publication August

28, 1991. From the Department of Pediatrics (Dr Deuel), Washington University School of Medicine, and the Department of Psychology (Ms Doar), Washington University School of Arts and Sciences, St Louis, MO. Address correspondence to Dr Deuel, Department of Pediatrics, Washington School of Medicine, St Louis Children’s Hospital, 400 South Kingshighway, Room 2S38, St Louis, MO 63110.

indicated damage to the brain (or &dquo;organicity&dquo;medical slang for ill-defined brain dysfunction) and that brain damage then explained the behavioral abnormalities of the child. 11-14 This neurologic argument is now fully reinforced by data showing that motor soft signs are no more indicative of fixed brain damage that any other neurobehavioral symp-

toms.l5-22 Charles Barlow 13 and others made the additional that effective clinical neurologic address of neurobehavioral symptoms required dissociation of one from another. This was to be followed by quantitative assessment of each symptom, using, of course, developmentally normative measures,23-25 and finally, by recommending remediation of each symptom appropriate to the weight of handicap it seemed to impose on the particular patient under

point

consideration.26-2s

Methods

.

In accordance with these principles, we undertook a study of manual praxis and dyspraxia among school-age children using a quantitative assay to text praxis. Manual dyspraxia is a motor performance deficit that may constitute, by itself, a severe handicap in childhood; 29-31 may give rise to

less-specific attention, learning,

and conduct

problems32 99

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that bring the child to the physician; and is not readily identified by routine neurologic history or examination.26 It may be defined as inability to learn or perform serial voluntary movements with the proficiency expected for age and/or verbal intelligence, in the absence of abnormalities of volition, strength, coordination, motor speed, or sensation that are sufficient to explain the poor performance.33

the medically referred clinic effect of was found on any subscale group group, (Figure 1). The two groups were therefore combined. Further analyses were carried out using post hoc t-tests that showed significant mean score differences among three age and sex groups. Performance on the test was best among 8- to 12-year-old boys (n 62), followed by 8- to 12-year-old girls (n = 28). Five- to 7-year-old children of both sexes (n = 74) were last. Improvement of motor performance with age has been found in previous studies.26 In order to directly compare these three age and sex groups that had been established empirically, we constructed z-scores for each group for the imitation of nonsense gestures, pantomime on command, and use of actual objects subscales and for the grand mean dyspraxia score. Next, we arbitrarily defined no

=

Test Items The items used for the

quantitative assay were assembled number of clinical sources, including the LincolnOseretsky Scales,34,35 and adapted from batteries to evaluate praxis in adults.36 All items were presented to each subject, and they were always presented in the same order. Following the traditional approach to testing apraxia in adults, they were divided into three subscales: (1) imitation of nonsense gestures, (2) pantomime on command, and (3) the use of actual objects. Each subscale score was the mean of all of its items, and the grand mean dyspraxia score was the mean of the three subscale scores. The scoring method allowed assessment of praxis scores in relationship to independent variables such as age and sex. Performance of each item was rated on a 5-point scale from excellent to totally unrecognizable performance (or no response). One hundred sixty-four test batteries were administered by four different individuals. Testers established interrater reliability with each other by simultaneously rating several subjects’ performance. The study was approved by the Washington University School of Medicine Human Studies Committee and the University City Public Schools. from

public school group and

a

dyspraxia

as a

grand

mean

dyspraxia

z-score one

standard deviation or more below the group mean. Under this empirical definition, there were 24 subjects with dyspraxia. Nineteen were from the group referred for medical evaluation because of poor school performance (24% of the referred children) and five were schoolchildren in regular classes (7% of the school subjects). X2 analysis shows the referred group to have a significantly higher percentage of dyspraxic subjects than the school group

Subjects The children tested

were

5 to 12 years old and

came

from

public primary school in a racially mixed, middle-class neighborhood (85 examinations), and outpatients referred to St Louis Children’s Hospital Psychology or Neurology Department for examination because of school problems (79 examinations). In both groups, parental consent was a precondition for participation. Of the schoolchildren, only those whose academic ratings from a two sources:

a

homeroom teacher were above average, average, or somewhat below average were tested. We excluded students rated &dquo;superior&dquo; or &dquo;clearly below average&dquo; in order to derive our normative data from children with average academic school performance. Of the clinic population, those with no evidence of static encephalopathy or mental retardation who were referred because of school problems were accepted. The two populations were of roughly similar racial and socioeconomic mix. These two a priori groups were originally selected for study so we could employ the new quantitative measure to make a more exacting comparison than had been possible with older, qualitative measures of praxis between the median normally progressing child and the child referred for medical attention because of trouble in school.

Results When an ANOVA

quantitative

scores



was

to

conducted using the raw differences between the

assess

FIGURE 1

Performance in terms of raw apraxia scores of the school group (average students in elementary grades) compared to the clinic group (elementary students referred to medical attention for school failure). No differences were found on any of three subscales. [However, when an empirical definition of dyspraxia was imposed, a significantly larger portion of clinic subjects (24%) than school subjects (7%) fulfilled it.]] ,

100

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(X2

10.8; P < .01). If we had made the requirement for dyspraxia more stringent, say performance two standard deviations or more below the mean, ten of the children (two girls and eight boys ranging in age from 6 to 12 years) would have qualified as dyspraxic, and all of them would have derived from the referred group. The findings thus uphold the notion that dyspraxia is of higher incidence in children referred to a medical facility because of school problems than in academically average schoolchildren. The original finding of no difference between these two groups is likely due to the interval level of quantitation yielded by the test, the improvement of measured performance with age, and the fact that the medically referred group was weighted toward older ages. Among those 24 children with overall (grand =

mean)

test

scores

showing dyspraxic performance,

looked for individuals whose subscale scores were dissociated along lines that would indicate ideational or ideomotor dyspraxia. Adopting definitions current in the literature, ideomotor apraxia was designated as failure to imitate gestures, with retained ability to use actual Difficulty with pantomime on command is used by some authorities as an additional requirement for ideomotor dyspraxia,39 so we adopted that as well and empirically required that an individual’s z-score on imitation of nonsense gestures and pantomime both be at least one standard deviation below that on use of actual objects. Three dyspraxic individuals, whose scores are plotted in Figure 2, fulfilled these criteria. For ideational apraxia, which most authorities we

objects. 37,38

-

FIGURE 2 Ideomotor

grand use

-

-

-

~~

_

z-scores of the three dyspraxic (ie, than -1) boys who performed well in

dyspraxia.

mean

of actual

nonsense

-

of less

objects but significantly worse

gestures and pantomime

ing they had

pure ideomotor

on

in imitation of

command, suggest-

dyspraxia.

One hundred

twenty-four batteries were accompanied by an IQ score or a teacher’s academic rating. These scores and ratings were used as an estimate of academic potential and were present for 16 of the 24 dyspraxics. Eleven of the 16 (66%) rated members of

define

as inability to employ common objects appropriately in the face of good ability to pantomime or imitate, 40-42 we required that the use of actual objects score be at least one standard deviation below both the imitation and pantomime scores. There were three dyspraxics who showed ideational dyspraxia. Their scores are plotted in Figure 3. Thus, by using a standardized quantitative test, capacities for carrying out complex motor sequences may be dissociated by the type of command to perform them. Among dyspraxics, the incapacity to perform similar motor behaviors under different task contingencies suggests that the elementary motor system is intact, but its efficiency differs, depending on the task requirements. At least, if under one requirement the hand and arm are perfectly capable of dexterously completing a motion, when at the next moment the same hand and arm cannot perform a

similar movement to a different command, it is hard to conclude that primary motility of the limb is defective.

FIGURE 3 Ideational apraxia. z-scores of three dyspraxic children who fulfilled the criterion of severely deficient performance in use of actual objects with relatively preserved performance on the other scales. Subject 23 was a 9-yearold male student rated as above average in academics by his teacher. Subject 7 was a 6-year-old male clinic patient with a Verbal IQ of 80, and subject 1 was a 7-year-old male clinic patient with no estimate of academic potential.

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the dyspraxic group were of average or better academic potential. When regression analyses were carried out using Full-Scale IQ scores (but not teacher ratings), among the 24 dyspraxics there was no relationship found between dyspraxia grand mean score and Full-Scale IQ score, while in the group as a whole, IQ correlated positively with praxis ability.43 One boy designated as dyspraxic had a Verbal IQ of 120, a Full-Scale IQ of 119, and a Performance IQ of 112. His grand mean dyspraxia score was the fourth lowest in the group (z 2.24). Thus, among dysacademic children, IQ (or potential) is highly praxic dissociated from motor performance capacities. =

Discussion In the limited

of motor

performance we investiuphold the neurologic findings gated, cited earlier concerning the dissociability of opinions area

our

seem

to

neurobehavioral symptoms within individuals. What does this imply in regard to representation of function in the brain? Rather than a diffuse representation of all neurobehavioral function in which one symptom is vaguely associated with another depending on the quantity of brain damage or dysfunction, dissociability suggests a model for representation of function-at least cognitive function-in the brain that allows for extremely discrete deficits.44 In 1926, Lashley45 promulgated the idea that the brain supports higher cortical functions by &dquo;mass action.&dquo; If sufficient quantity of the brain was affected, irrespective of where, then brain functions would deteriorate. This model of representation of brain function was current in the middle part of the 20th century and may have provided the grounds for the notion that motor soft signs were indicative of brain damage somewhere or somehow. Clearly, this model cannot accommodate the present find-

ings. In order to

concerning

explain the clinical and research facts

motor execution deficits in children with

neurobehavioral disorders, a new theoretical model is required. It must allow an explanation of how the central nervous system supports functions such as voluntarily directed motor behavior and attention, communication and language use, memory, and learning. Models have been described with properties that would be more compatible with observed dissociable disorders among these higher mental functions .46-48 Mesulam49 recently proposed multifocal networks as the substratum that supports higher cortical functions in the brain. These networks process information in parallel, both anatomi-

cally and temporally, and interact with each other at multiple neuroanatomic sites. In addition, the sites of interaction may be configured by the functional demand of the task at hand, and may be limited by the functional demands of other tasks simultaneously being processed by the central nervous system. Thus, at different times, a single anatomic substrate may be active in radically different functions.’o Such a model provides the requisite flexibility and discreteness to account for the clinical observations that have been accruing concerning motor and other soft signs in childhood neurobehavioral disorders. Thus, as deduced early on from neurologic experience by Dr Barlowl3 and others,ll-14 dyspraxia and other motor performance deficits are of high incidence in children with neurobehavioral complaints but do not provide evidence for fixed brain damage or static dysfunction. Study of the dyspraxias and their possible dissociations may, however, help to provide detailed insights into the way the brain normally constructs its plans for motor performance. From that point, the as-yet-undescribed encephalopathic processes that lead to dissociable performance deficits may be understood. Then at last, by learning how these behaviors are processed to completion in the central nervous system, we may attain optimal methods for alleviating the difficulties created in everyday living for children with motor skill disorders.

Acknowledgments to Adam’s Fund for financial support, to teachers, parents, and subjects for their participation, and to Jo

We

are

Ballard for

grateful

typing

the

manuscript.

References

schizophrenia: Clinical study of one hundred schizophrenic children. Am J Orthopsychiatry 1947; 17:40-46. 2. Kanner L: Autistic disturbances of affective contact. Nerv Child 1943;2:217-250. 3. Kennard MA: Value of equivocal signs in neurologic diagno1. Bender L: Childhood

sis. Neurology 1960;10:753-764. 4. Orton S: "Word-blindness" in school children. Arch Neurol

1925;14:582- 615. 5. Strauss A, Leitinen NC: Psychopathology and Education of the Brain Injured Child. New York, Grune & Stratton, 1947. 6. Prechtl H, Stemmer C: The choreiform syndrome in children. Dev Med Child Neurol 1962;4:119-127. 7. Belmont L, Birch H: Lateral dominance, lateral awareness, and reading disabilities. Child Dev 1965;36:57-71. 8. Clements S: Minimal Brain Dysfunction in Children. USPHS Publication 141. Washington DC, US Government Printing Office, 1966.

102

Downloaded from jcn.sagepub.com at UNIV OF ILLINOIS URBANA on March 16, 2015

9. Roach

E, Kephart N: The Purdue Perceptual Motor Survey. Columbus, OH, Charles C. Merrill, 1966. 10. Hertzig M, Bortner M, Birch H: Neurologic findings in chil-

31.

dren 11. 12. 13.

educationally designated as "brain-damaged." AmJ Orthopsychiatry 1969;39:437-446. Gomez M: Minimal cerebral dysfunction (maximal neurologic confusion). Clin Pediatr 1967;6:589-591. 1973;15:527-530. Ingram T: Soft signs. Dev Med Child Neurol Barlow CF: "Soft signs" in children with learning disorders.

32.

33.

AmJ Dis Child 1974;128:605-606. 14. Touwen B, Sporrell T: Soft signs and MBD. Dev Med Child Neurol 1979;21:528-530. P, Chen T: Minimal Brain Dysfunction: A Prospective Study. Hillsdale, NY, Lawrence Earlbaum, 1981. 16. Rutter M: Psychological sequelae of brain damage in children.

34.

15. Nichols

35.

AmJ Psychiatry 1981;33:845-853. 17. Rutter M: Symptoms attributed to minimal brain damage in children. Am J Psychiatry 1982;134:21-33. 18. Rutter M: Introductions: Concepts of brain dysfunction syndromes, in Rutter M (ed): Developmental Neuropsychiatry. New York, Guilford, 1983, pp 259-279. 19. Denckla M, LeMay M, Chapman C: Few CT scan abnormalities found even in neurologically impaired learning disabled children. J Learning Disabil 1985;18:132-135. 20. Peters J: A special neurological examination for school aged children. In Tupper D (ed): Soft Neurological Signs. New York, Grune & Stratton, 1987, pp 370-371. 21. Taylor H: The meaning and value of soft neurological signs in the behavioral sciences, in Tupper D (ed): Soft Neurological Signs. New York, Grune & Stratton, 1987, pp 297-335. 22. Bigler E: The role of neuropsychological assessment in relation to other types of assessments with children, in Tramantana MG, Hooper SR (eds): Assessment Issues in Child Neuropsychology. New York, Plenum Press, 1988, p 75. 23. Costa L, Scarola L, Rapin I: Purdue pegboard scores for normal grammar school children. Percept Mot Skills 1964; 18:748-755. 24. Tallal P, Stark R, Mellitis D: The relationship between auditory temporal analysis and receptive language development. 25.

26. 27.

28. 29.

30.

Neuropsychologia 1985;23:527-534. Dewey D, Roy E, Square-Storer P, Hayden D: Limb and oral praxia abilities of children with verbal sequencing deficits. Dev Med Child Neurol 1988;30:743-751. Gubbay S: The management of the clumsy child. Dev Med

Child Neurol 1978;20:643-646. Satterfield J, Satterfield B, Cantwell D: Three year multimodality treatment of 100 hyperactive boys. J Pediatr 1981; 98:650-655. Deuel RK, Doar BP: Testing manual praxis in school children, abstract. Ann Neurol 1990;28:425-426. Gubbay S: The Clumsy Child: A Study of Developmental Apraxic and Agonistic Ataxia. London, WB Saunders, 1975. Quitkin F, Rifkin A, Klein D: Neurologic soft signs in schizo-

36.

phrenia and character disorders. Arch Gen Psychiatry 1976; 33:845-853. Gordon N, McKinley I: Helping Clumsy Children. New York, Churchill Livingstone, 1980. Annell A: School problems in children of average or superior intelligence. A preliminary report.J Ment Sci 1949;95:901-909. David R, Deuel R, Ferry P, et al: Proposed Neurology of Disorders of Higher Cerebral Function in Children. Task Force on Nosology of Disorders on Higher Cerebral Function in Children. Child Neurological Society, Minneapolis, MN, 1981. Oseretsky N: Methoden der Untersuchung der Motorick, Heft 57. Beiheft zur Zeitschrift für angewandte Psychologie. Leipzig, Barth, 1931. Sloan W: The Lincoln Adaptation of the Oseretsky Tests: A Measure of Motor Proficiency. Lincoln, IL, Lincoln State School & Colony, 1948. Edwards DF, Deuel RK, Baum CM, Morris J: A quantitative analysis of apraxia in senile dementia of the Alzheimer type: Stage related differences in prevalence and type. Dementia, in

press. 37. DeRenzi E, Motti F, Nichelli P: Imitating gestures: A quantitative approach to ideomotor apraxia. Arch Neurol 1980;37:6-10. 38. Basso A, Capitani E, Della-Sala SD, et al: Ideomotor apraxia: A study of initial severity. Acta Neurol Scand 1987;76:142-146. 39. Kertesz A, Hooper P: Praxis and language: The extent and variety of apraxia in aphasia. Neuropsychologia 1982;20:275-286. 40. DeRenzi E, Pieczuro A, Vignolo LA: Ideational apraxia: A

quantitative study. Neuropsychologia 1966;6:41-52. 41. DeRenzi E, Lucchelli F: Ideational apraxia. Brain 1988; 111:1173-1185. 42. Poeck K, Lehmkuhl G: Ideatory apraxia in a left-handed patient with right-sided brain lesion. Cortex 1980;16:273-284. 43. Deuel RK, Doar BP: Testing manual praxis in school children, abstract. Ann Neurol 1990;28:425-426. 44. Shallice T: Neurological impairment of cognitive processing. Br Med Bull 1981;37:187-192. 45. Lashley KS: Brain Mechanisms and Intelligence. Chicago, University of Chicago Press, 1929, pp 157-176. 46. Deeke L, Kornhuber H, Lang W, et al: Timing function of frontal cortex in motor tasks. Hum Neurobiol 1985;4:143-154. 47. Gevins A: Distributed neuroelectric patterns of human neocortex during simple cognitive tasks. Prog Brain Res 1990;

85:337-355. 48. Mesulam MM: A cortical network for directed attention and unilateral neglect. Ann Neurol 1981;10:309-325. 49. Mesulam MM: Large scale neurocognitive networks and distributed processing for attention, language, memory. Ann 50.

Neurol 1990;28:597-613. Getting PA, Dekin MS: Mechanisms of pattern generation underlying swimming in Tritonia. IV: Gating of central pattern generator. J Neurophysiol 1985;53:466-480.

103

Downloaded from jcn.sagepub.com at UNIV OF ILLINOIS URBANA on March 16, 2015

Developmental manual dyspraxia: a lesson in mind and brain.

For decades, pediatricians assiduously documented "soft neurologic signs" in children referred for school learning difficulties, although pediatric ne...
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