Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-20T00:56:18.507Z Has data issue: false hasContentIssue false

Developmental dyspraxia is not limited to imitation in children with autism spectrum disorders

Published online by Cambridge University Press:  17 May 2006

STEWART H. MOSTOFSKY
Affiliation:
Department of Developmental Cognitive Neurology, Kennedy Krieger Institute, Baltimore, Maryland Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland Department of Psychiatry, Johns Hopkins University School of Medicine, Baltimore, Maryland
PRACHI DUBEY
Affiliation:
F.M. Kirby Research Center, Kennedy Krieger Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland
VANDNA K. JERATH
Affiliation:
Department of Developmental Cognitive Neurology, Kennedy Krieger Institute, Baltimore, Maryland
EVA M. JANSIEWICZ
Affiliation:
Department of Developmental Cognitive Neurology, Kennedy Krieger Institute, Baltimore, Maryland
MELISSA C. GOLDBERG
Affiliation:
Department of Developmental Cognitive Neurology, Kennedy Krieger Institute, Baltimore, Maryland Department of Psychiatry, Johns Hopkins University School of Medicine, Baltimore, Maryland
MARTHA B. DENCKLA
Affiliation:
Department of Developmental Cognitive Neurology, Kennedy Krieger Institute, Baltimore, Maryland Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland Department of Psychiatry, Johns Hopkins University School of Medicine, Baltimore, Maryland Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Maryland

Abstract

Impaired imitation of skilled gestures is commonly reported in autism. Questions, however, remain as to whether impaired imitation is associated with a more generalized deficit in performance of gestures consistent with a dyspraxia and whether the pattern of errors differs from that observed in typically developing children. To address these questions, praxis in 21 high-functioning children with autism spectrum disorders (ASD) was compared with 24 typically developing controls using a traditional approach in which performance was evaluated through detailed examination of error types. Children with ASD produced significantly fewer correct responses not only during Gesture to Imitation, but also during Gesture to Command and with Tool Use. The pattern of errors in ASD was similar to that of controls with spatial errors being most common in both groups; however, body-part-for-tool errors were more common in children with ASD, suggesting dyspraxia is not entirely attributable to motor deficits. The findings suggest that autism is associated with a generalized praxis deficit, rather than a deficit specific to imitation. In a developmental disorder such as autism, the findings may reflect abnormalities in frontal/parietal–subcortical circuits important for acquisition (i.e., learning) of sensory representations of movement and/or the motor sequence programs necessary to execute them. (JINS, 2006, 12, 314–326.)

Type
Research Article
Copyright
© 2006 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bailey, A., Luthert, P., Dean, A., Harding, B., Janota, I., Montgomery, M., Rutter, M., & Lantos, P. (1998). A clinicopathological study of autism. Brain, 121, 889905.CrossRefGoogle Scholar
Bauman, M. & Kemper, T. (1994). Neuroanatomic observations of the brain in autism. Baltimore: Johns Hopkins University Press.
Bland, J.M. & Altman, D.G. (1986). Statistical methods for assessing agreement between two methods of clinical measurement. The Lancet, 1, 307310.Google Scholar
Cermak, S.A. (1985). Developmental dyspraxia. In E. Roy (Ed.), Neuropsychological studies of apraxia and related disorders (pp. 225243). Amsterdam: North-Hollans.
Cermak, S.A., Coster, W., & Drake, C. (1980). Representational and nonrepresentational gestures in boys with learning disabilities. American Journal of Occupational Therapy, 34, 1926.Google Scholar
Churchill, D. (1978). Language of autistic children. New York: V.H. Winston & Sons.
Churchill, D.W. (1972). The relation of infantile autism and early childhood schizophrenia to developmental language disorders of childhood. Journal of Autism and Childhood Schizophrenia, 2, 182197.CrossRefGoogle Scholar
Clark, M.A., Merians, A.S., Kothari, A., Poizner, H., Macauley, B., Gonzalez Rothi, L.J., & Heilman, K.M. (1994). Spatial planning deficits in limb apraxia. Brain, 117, 10931106.CrossRefGoogle Scholar
Cohen, J., Cohen, P., West, S.G., & Aiken, L.S. (2002). Applied multiple regression/correlation analyses in the behavioral sciences. Mahwah, NJ: Lawrence Erlbaum Associates.
Daselaar, S.M., Rombouts, S.A., Veltman, D.J., Raaijmakers, J.G., & Jonker, C. (2003). Similar network activated by young and old adults during the acquisition of a motor sequence. Neurobiology of Aging, 24, 10131019.CrossRefGoogle Scholar
De Renzi, E., Motti, F., & Nichelli, P. (1980). Imitating gestures. A quantitative approach to ideomotor apraxia. Archives of Neurology, 37, 610.Google Scholar
DeMyer, M., Alpern, G., Barton, S., DeMyer, W., Churchill, D., Hingtgen, J., Bryson, C., Pontius, W., & Kimberlin, C. (1972). Imitation in autistic, early schizophrenic, and non-psychotic subnormal children. Journal of Autism and Childhood Schizophrenia, 2, 264287.CrossRefGoogle Scholar
DeMyer, M.K., Hingtgen, J.N., & Jackson, R.K. (1981). Infantile autism reviewed: A decade of research. Schizophrenia Bulletin, 7, 388451.Google Scholar
Denckla, M.B. & Roeltgen, D.P. (1992). Disorders of motor function and control. In F. Boller & J. Grafman (Eds.), Handbook of neuro-psychology, Vol. 6 (pp. 455476). Amsterdam, The Netherlands: Elsevier Science Publishers.
Dewey, D. (1993). Error analysis of limb and orofacial praxis in children with developmental motor deficits. Brain and Cognition, 23, 203221.Google Scholar
Dewey, D. & Kaplan, B.J. (1992). Analysis of praxia task demands in the assessment of children with developmental motor deficits. Developmental Neuropsychology, 8, 367379.Google Scholar
Doyon, J., Penhune, V., & Ungerleider, L.G. (2003). Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia, 41, 252262.Google Scholar
Efron, B. & Tibshirani, R.J. (1993). An introduction to the bootstrap. New York: Chapman & Hall.CrossRef
Fatemi, S.H., Halt, A.R., Realmuto, G., Earle, J., Kist, D.A., Thuras, P., & Merz, A. (2002). Purkinje cell size is reduced in cerebellum of patients with autism. Cellular and Molecular Neurobiology, 22, 171175.Google Scholar
Ghaziuddin, M. & Butler, E. (1998). Clumsiness in autism and Asperger syndrome: A further report. Journal of Intellectual Disability Research: JIDR, 42, 4348.CrossRefGoogle Scholar
Ghilardi, M.F., Ghez, C., Dhawan, V., Moeller, J., Mentis, M., Nakamura, T., Antonini, A., & Eidelberg, D. (2000). Patterns of regional brain activation associated with different forms of motor learning. Brain Research, 871, 127145.Google Scholar
Gonzales Rothi, L.J., Raymer, A.M., & Heilman, K.M. (1997). Limb praxis assessment. In L.J. Gonzales Rothi & K.M. Heilman (Eds.), Apraxia: The cognitive neuropsychology of praxis. Hove, UK: Psychology Press.
Grafton, S.T., Hazeltine, E., & Ivry, R.B. (1998). Abstract and effector-specific representations of motor sequences identified with PET. Journal of Neuroscience, 18, 94209428.Google Scholar
Green, D., Baird, G., Barnett, A.L., Henderson, L., Huber, J., & Henderson, S.E. (2002). The severity and nature of motor impairment in Asperger's syndrome: A comparison with specific developmental disorder of motor function. Journal of Child Psychology and Psychiatry, 43, 655668.CrossRefGoogle Scholar
Gubbay, S.S. (1975). Clumsy children in normal schools. Medical Journal of Australia, 1, 233236.Google Scholar
Haas, R., Townsend, J., Courchesne, E., Lincoln, A., Schriebman, L., & Yeung-Courchesne, R. (1996). Neurologic abnormalities in infantile autism. Journal of Child Neurology, 11, 8492.Google Scholar
Hallett, M., Lebiedowska, M.K., Thomas, S.L., Stanhope, S.J., Denckla, M.B., & Rumsey, J. (1993). Locomotion of autistic adults. Archives of Neurology, 50, 13041308.Google Scholar
Hammes, J. & Langdell, T. (1981). Precursors of symbol formation and childhood autism. Journal of Autism and Developmental Disorders, 11, 331346.CrossRefGoogle Scholar
Hanna-Pladdy, B., Daniels, S.K., Fieselman, M.A., Thompson, K., Vasterling, J.J., Heilman, K.M., & Foundas, A.L. (2001a). Praxis lateralization: Errors in right and left hemisphere stroke. Cortex, 37, 219230.Google Scholar
Hanna-Pladdy, B., Heilman, K.M., & Foundas, A.L. (2001b). Cortical and subcortical contributions to ideomotor apraxia: Analysis of task demands and error types. Brain, 124, 25132527.Google Scholar
Heilman, K.M. & Gonzalez Rothi, L.J. (2003). Apraxia. In K.M.H. a. E. Valenstein (Ed.), Clinical neuropsychology, 4th ed. (pp. 215235). New York: Oxford University Press.
Hertzig, M., Snow, M., & Sherman, M. (1989). Affect and cognition in autism. Journal of the American Association for Child and Adolescent Psychiatry, 28, 195199.Google Scholar
Hill, E.L. (1998). A dyspraxic deficit in specific language impairment and developmental coordination disorder? Evidence from hand and arm movements. Developmental Medicine and Child Neurology, 40, 388395.Google Scholar
Jacobs, D.H., Adair, J.C., Williamson, D.J., Na, D.L., Gold, M., Foundas, A.L., Shuren, J.E., Cibula, J.E., & Heilman, K.M. (1999a). Apraxia and motor-skill acquisition in Alzheimer's disease are dissociable. Neuropsychologia, 37, 875880.Google Scholar
Jacobs, D.H., Adair, J.C., Macauley, B., Gold, M., Gonzalez Rothi, L.J., & Heilman, K.M. (1999b). Apraxia in corticobasal degeneration. Brain and Cognition, 40, 336354.Google Scholar
Jansiewicz, E., Goldberg, M.C., Newschaffer, C.J., Denckla, M.B., Landa, R.J., & Mostofsky, S.H. (2006). Motor signs distinguish children with high functioning autism and Asperger's syndrome from controls. Journal of Autism and Developmental Disorders, (in press).CrossRefGoogle Scholar
Jones, V. & Prior, M. (1985). Motor imitation ability and neurological signs in autistic children. Journal of Autism and Developmental Disorders, 15, 3746.CrossRefGoogle Scholar
Kaplan, E. (1968). Gestural representation of implement usage: An organic-developmental study. Ph.d. Thesis, Clarke University, Massachusetts.
Kaplan, E. (1983). Process and achievement revisited. In S.W.E. Kaplan (Ed.), Toward a holistic developmental psychology (pp. 143157). Hillsboro, NJ: Erlbaum.
Koenker, R. & Bassett, G. (1978). Regression qualities. Econometrica, 46, 3350.CrossRefGoogle Scholar
Lord, C., Risi, S., Lambrecht, L., Cook, E.H.J., Leventhal, B.L., DiLavore, P.C., Pickles, A., & Rutter, M. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205223.Google Scholar
Lord, C., Rutter, M., Goode, S., Heemsbergen, J., Jordan, H., Mawhood, L., & Schopler, E. (1989). Autism diagnostic observation schedule: A standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19, 185212.Google Scholar
Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism Diagnostic Interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659685.Google Scholar
Manjiviona, J. & Prior, M. (1995). Comparison of Asperger syndrome and high-functioning autistic children on a test of motor impairment. Journal of Autism and Developmental Disorders, 25, 2339.Google Scholar
Merians, A.S., Clark, M., Poizner, H., Jacobs, D.H., Adair, J.C., Macauley, B., Gonzales Rothi, L.J., & Heilman, K.M. (1999). Apraxia differs in corticobasal degeneration and left-parietal stroke: A case study. Brain and Cognition, 40, 314335.Google Scholar
Mostofsky, S.H., Goldberg, M.C., Landa, R.J., & Denckla, M.B. (2000). Evidence for a deficit in procedural learning in children and adolescents with autism: Implications for cerebellar contribution. Journal of the International Neuropsychological Society, 6, 752759.Google Scholar
Muller, R.A., Kleinhans, N., Pierce, K., Kemmotsu, N., & Courchesne, E. (2002). Functional MRI of motor sequence acquisition: Effects of learning stage and performance. Brain Research. Cognitive Brain Research, 14, 277293.Google Scholar
Ohgami, Y., Matsuo, K., Uchida, N., & Nakai, T. (2004). An fMRI study of tool-use gestures: Body part as object and pantomime. Neuroreport, 15, 19031909.CrossRefGoogle Scholar
Ohta, M. (1987). Cognitive disorders of infantile autism: A study employing the WISC, spatial relationships, conceptualization, and gesture imitations. Journal of Autism and Developmental Disorders, 17, 4562.Google Scholar
Overton, W. & Jackson, J. (1973). The representation of imagined objects in action sequences: A developmental study. Child Development, 44, 309314.CrossRefGoogle Scholar
Pharr, V., Uttl, B., Stark, M., Litvan, I., Fantie, B., & Grafman, J. (2001). Comparison of apraxia in corticobasal degeneration and progressive supranuclear palsy. Neurology, 56, 957963.Google Scholar
Poizner, H., Clark, M.A., Merians, A.S., Macauley, B., Gonzalez Rothi, L.J., & Heilman, K.M. (1995). Joint coordination deficits in limb apraxia. Brain, 118, 227242.Google Scholar
Rapin, I. (1991). Autistic children: Diagnosis and clinical features. Pediatrics, 87, 751760.Google Scholar
Ritvo, E.R., Freeman, B.J., Scheibel, A.B., Duong, T., Robinson, H., Guthrie, D., et al. (1986). Lower Purkinje cell counts in the cerebella of four autistic subjects: Initial findings of the UCLA-NSAC autopsy research report. American Journal of Psychiatry, 143, 862866.Google Scholar
Rogers, S. & Pennington, B. (1991). A theoretical approach to the deficits in infantile autism. Development and Psychopathology, 3, 137163.Google Scholar
Rogers, S., Bennetto, L., McEvoy, R., & Pennington, B. (1996). Imitation and pantomime in high-functioning adolescents with autism spectrum disorders. Child Development, 67, 20602073.Google Scholar
Rogers, S.J., Hepburn, S.L., Stackhouse, T., & Wehner, E. (2003). Imitation performance in toddlers with autism and those with other developmental disorders. Journal of Child Psychology and Psychiatry, 44, 763781.Google Scholar
Roy, E.A., Elliott, D., Dewey, D., & Square-Storer, P. (1990). Impairments to praxis and sequencing in adult and developmental disorders. Columbia, SC: University of South Carolina Press.
Schendan, H.E., Searl, M.M., Melrose, R.J., & Stern, C.E. (2003). An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron, 37, 10131025.Google Scholar
Smith, I.M. & Bryson, S.E. (1994). Imitation and action in autism: A critical review. Psychological Bulletin, 116, 259273.Google Scholar
Stone, W.L., Ousley, O.Y., & Littleford, C.L. (1997). Motor imitation in children with autism: What's the object? Journal of Abnormal Child Psychology, 25, 275485.Google Scholar
Szatmari, P., Archer, L., Fisman, S., Streiner, D.L., & Wilson, F. (1995). Asperger's syndrome and autism: Differences in behavior, cognition, and adaptive functioning. Journal of the American Academy of Child and Adolescent Psychiatry, 34, 16621671.CrossRefGoogle Scholar
Teitelbaum, P., Teitelbaum, O., Nye, J., Fryman, J., & Maurer, R.G. (1998). Movement analysis in infancy may be useful for early diagnosis of autism. Proceedings of National Academy of Science of the United States of America, 95, 1398213987.Google Scholar
Thal, D., Tobias, S., & Morrison, D. (1991). Language and gesture in late talkers: A 1-year follow-up. Journal of Speech and Hearing Research, 34, 604612.Google Scholar
Vilensky, J.A., Damasio, A.R., & Maurer, R.G. (1981). Gait disturbance in patients with autistic behavior. Archives of Neurology, 38, 646649.Google Scholar
Wechsler, D. (1974). Wechsler Intelligence Scale for Children-Revised [WISC-R]. New York: Psychological Corporation.
Wechsler, D. (1991). Wechsler Intelligence Scale for Children-III. San Antonio, TX: The Psychological Corporation.
Williams, J.H., Whiten, A., & Singh, T. (2004). A systematic review of action imitation in autistic spectrum disorder. Journal of Autism and Developmental Disorders, 34, 285299.Google Scholar
Williams, J.H., Whiten, A., Suddendorf, T., & Perrett, D.I. (2001). Imitation, mirror neurons and autism. Neuroscience and Biobehavioral Reviews, 25, 287295.Google Scholar
Williams, R.S., Hauser, S.L., Purpura, D.P., DeLong, G.R., & Swisher, C.N. (1980). Autism and mental retardation: Neuropathologic studies performed in four retarded persons with autistic behavior. Archives of Neurology, 37, 749753.CrossRefGoogle Scholar
Wing, L. (1969). The handicaps of autistic children—a comparative study. Journal of Child Psychology and Psychiatry, 10, 140.Google Scholar
Zoia, S., Pelamatti, G., Cuttini, M., Casotto, V., & Scabar, A. (2002). Performance of gesture in children with and without DCD: Effects of sensory input modalities. Developmental Medicine and Child Neurology, 44, 699705.Google Scholar