Abstract
Abnormalities in motor skills have been regarded as part of the symptomatology characterizing autism spectrum disorder (ASD). It has been estimated that 80 % of subjects with autism display “motor dyspraxia” or clumsiness that are not readily identified in a routine neurological examination. In this study we used behavioral measures, event-related potentials (ERP), and lateralized readiness potential (LRP) to study cognitive and motor preparation deficits contributing to the dyspraxia of autism. A modified Posner cueing task was used to analyze motor preparation abnormalities in children with autism and in typically developing children (N = 30/per group). In this task, subjects engage in preparing motor response based on a visual cue, and then execute a motor movement based on the subsequent imperative stimulus. The experimental conditions, such as the validity of the cue and the spatial location of the target stimuli were manipulated to influence motor response selection, preparation, and execution. Reaction time and accuracy benefited from validly cued targets in both groups, while main effects of target spatial position were more obvious in the autism group. The main ERP findings were prolonged and more negative early frontal potentials in the ASD in incongruent trials in both types of spatial location. The LRP amplitude was larger in incongruent trials and had stronger effect in the children with ASD. These effects were better expressed at the earlier stages of LRP, specifically those related to response selection, and showed difficulties at the cognitive phase of stimulus processing rather that at the motor execution stage. The LRP measures at different stages reflect the chronology of cognitive aspects of movement preparation and are sensitive to manipulations of cue correctness, thus representing very useful biomarker in autism dyspraxia research. Future studies may use more advance and diverse manipulations of movement preparation demands in testing more refined specifics of dyspraxia symptoms to investigate functional connectivity abnormalities underlying motor skills deficits in autism.
Similar content being viewed by others
References
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text revision). Washington, DC: American Psychiatric Press.
Asperger, H. (1944). Die „Autistischen Psychopathen” im Kindesalter. Archiv für Psychiatrie und Nervenkrankheiten, 117, 76–136.
Belmonte, M. K., Allen, G., Beckel-Mitchener, A., Boulanger, L. M., Carper, R. A., & Webb, S. J. (2004). Autism and abnormal development of brain connectivity. The Journal of Neuroscience, 24(2), 9228–9231.
Brian, J., Bryson, S. E., Garon, N., Roberts, W., Smith, I. M., Szatmari, P., & Zwaigenbaum, L. (2008). Clinical assessment of autism in high-risk 18-month-olds. Autism, 12(5), 433–456.
Casanova, M. F., El-Baz, A., Mott, M., Mannheim, G., Hassan, H., Fahmi, R., et al. (2009). Reduced gyral window and corpus callosum size in autism: Possible macroscopic correlates of a minicolumnopathy. Journal of Autism and Developmental Disorders, 39(5), 751–764.
Casanova, M. F., van Kooten, I. A., Switala, A. E., van Engeland, H., Heinsen, H., Steinbusch, H. W., et al. (2006). Minicolumnar abnormalities in autism. Acta Neuropathologica, 112(3), 287–303.
Coles, M. G. (1989). Modern mind-brain reading: Psychophysiology, physiology, and cognition. Psychophysiology, 26(3), 251–269.
Cummings, J. L. (1998). Frontal-subcortical circuits and human behavior: Commentary. Journal of Psychosomatic Research, 44, 627–628.
Dowell, L. R., Mahone, E. M., & Mostofsky, S. H. (2009). Association of postural knowledge and basic motor skill with dyspraxia in autism: Implication for abnormalities in disturbed connectivity and motor learning. Neuropsychology, 23(5), 563–570.
Dziuk, M. A., Gidley Larson, J. C., Apostu, A., Mahone, E. M., Denckla, M. B., & Mostofsky, S. H. (2007). Dyspraxia in autism: Association with motor, social, and communicative deficits. Developmental Medicine and Child Neurology, 49(10), 734–739.
Eimer, M. (1998). The lateralized readiness potential as an on-line measure of central response activation processes. Behavior Research Methods, Instruments, & Computers, 30(1), 146–156.
Elliott, R. (2003). Executive functions and their disorders. British Medical Bulletin, 65, 49–59.
Fan, Y. T., Decety, J., Yang, C. Y., Liu, J. L., & Cheng, Y. (2010). Unbroken mirror neurons in autism spectrum disorders. Journal of Child Psychology and Psychiatry, 51(9), 981–988.
Faw, B. (2003). Pre-frontal executive committee for perception, working memory, attention, long-term memory, motor control, and thinking: A tutorial review. Consciousness and Cognition, 12, 83–139.
Fuentes, C. T., Mostofsky, S. H., & Bastian, A. J. (2011). No proprioceptive deficits in autism despite movement-related sensory and execution impairments. Journal of Autism and Developmental Disorders, 41(10), 1352–1361.
Fuster, J. M. (1997). The prefrontal cortex: Anatomy, physiology, and neuropsychology of the rontal lobe (3rd ed.). Philadelphia: Lippincott-Raven.
Fuster, J. M. (1999). Cognitive functions of the frontal lobes. In B. L. Miller & J. L. Cummings (Eds.), Human frontal lobes (pp. 187–195). New York: Guilford.
Fuster, J. M. (2001). The prefrontal cortex—An update: Time is of the essence. Neuron, 30(2), 319–333.
Geschwind, D. H., & Iacoboni, M. (1999). Structural and functional asymmetries of the human frontal lobes. In B. L. Miller & J. L. Cummings (Eds.), Human frontal lobes (pp. 45–70). New York: Guilford.
Gibbs, J., Appleton, J., & Appleton, R. (2007). Dyspraxia or developmental coordination disorder. Unraveling the enigma. Archives of Disease in Childhood, 92(6), 534–539.
Gidley Larson, J. C., & Mostofsky, S. H. (2006). Motor deficits in autism. In R. Tuchman & I. Rapin (Eds.), Autism: A neurological disorder of early brain development (pp. 231–247). London: MacKeith Press.
Golob, E. J., Pratt, H., & Starr, A. (2002). Preparatory slow potentials and event-related potentials in an auditory cued attention task. Clinical Neurophysiology, 113, 1544–1557.
Gowen, E., & Hamilton, A. (2013). Motor abilities in autism: A review using a computational context. Journal of Autism and Developmental Disorders, 43(2), 323–344.
Gratton, G., Coles, M. G., Sirevaag, E. J., Eriksen, C. W., & Donchin, E. (1988). Pre- and poststimulus activation of response channels: A psychophysiological analysis. Journal of Experimental Psychology: Human Perception and Performance, 14(3), 331–344.
Hamilton, A. (2008). Emulation and mimicry for social interaction: A theoretical approach to imitation in autism. Quarterly Journal of Experimental Psychology, 61, 101–115.
Hamilton, A., Brindley, R., & Frith, U. (2007). Imitation and action understanding in autistic spectrum disorders: How valid is the hypothesis of a deficit in the mirror neuron system? Neuropsychologia, 45, 1859–1868.
Heilman, K. M., & Rothi, L. J. (1993). Apraxia. In K. Heilman & E. Valstein (Eds.), Clinical neuropsychology (3rd ed., pp. 141–163). New York: Oxford University Press.
Herbert, M. R., Ziegler, D. A., Makris, N., Filipek, P. A., Kemper, T. L., Normandin, J. J., et al. (2004). Localization of white matter volume increase in autism and developmental language disorder. Annals of Neurology, 55, 530–540.
Hill, E. L. (2004). Evaluating the theory of executive dysfunction in autism. Developmental Review, 24, 189–233.
Hill, E. L., & Frith, U. (2003). Understanding autism: Insights from mind and brain. Philosophical Transactions of the Royal Society London, B, 358, 281–289.
Hoshiyama, M., Kakigi, R., Berg, P., Koyama, S., Kitamura, Y., & Shimojo, M. (1997). Identification of motor and sensory brain activities during unilateral finger movement: Spatiotemporal source analysis of movement-associated magnetic fields. Experimental Brain Research, 115, 6–14.
Iverson, J. M., & Braddock, B. A. (2011). Links between language, gesture, and motor skill in children with language impairment. Journal of Speech, Language, and Hearing Research, 54(1), 72–86.
Jahanshahi, M., & Hallet, M. (2003). Bereitschaftspotential: Movement-related cortical potentials. New York: Kluwer Academic.
Jansiewicz, E. M., Goldberg, M. C., Newschaffer, C. J., Denckla, M. B., Landa, R., & Mostofsky, S. H. (2006). Motor signs distinguish children with high functioning autism and Asperger’s syndrome from controls. Journal of Autism and Developmental Disorders, 36, 613–621.
Just, M. A., Cherkassky, V. L., Keller, T. A., Kana, R. K., & Minshew, N. J. (2007). Functional and anatomical cortical underconnectivity in autism: Evidence from an fMRI study of an executive function task and corpus callosum morphomtery. Cerebral Cortex, 17(4), 951–961.
Kanner, L. (1943). Autistic disturbances of affective contact. Nervous Child, 2, 217–250.
Kawamura, M., & Mochizuki, S. (1999). Primary progressive apraxia. Neuropathology, 19, 249–258.
Koshino, H., Carpenter, P. A., Minshew, N. J., Cherkassky, V. L., Keller, T. A., & Just, M. A. (2005). Functional connectivity in an fMRI working memory task in high-functioning autism. Neuroimage, 24(3), 810–821.
Le Couteur, A., Lord, C., & Rutter, M. (2003). The autism diagnostic interview-revised (ADI-R). Los Angeles, CA: Western Psychological Services.
Leighton, J., Bird, G., Charman, T., & Heyes, C. (2008). Weak imitative performance is not due to a functional ‘mirroring’ deficit in adults with autism spectrum disorders. Neuropsychologia, 46, 1041–1049.
Leuthold, H., & Jentzsch, I. (2001). Neural correlates of advance movement preparation: A dipole source analysis approach. Brain Research. Cognitive Brain Research, 12(2), 207–224.
Leuthold, H., Sommer, W., & Ulrich, R. (2004). Preparing for action: Inferences from CNV and LRP. Journal of Psychophysiology, 18, 77–88.
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(2), 185–212.
MacNeil, L. K., & Mostofsky, S. H. (2012). Specificity of dyspraxia in children with autism. Neuropsychology, 26(2), 165–171.
Ming, X., Brimacombe, M., & Wagner, G. C. (2007). Prevalence of motor impairment in autism spectrum disorders. Brain & Development, 29(9), 565–570.
Mostofsky, S. H., Dubey, P., Jerath, V. K., Jansiewicz, E. M., Goldberg, M. C., & Denckla, M. B. (2006). Developmental dyspraxia is not limited to imitation in children with autism spectrum disorders. Journal of the International Neuropsychological Society, 12(3), 314–326.
Mottron, L., Burack, J. A., Iarocci, G., Belleville, S., & Enns, J. T. (2003). Locally oriented perception with intact global processing among adolescents with high-functioning autism: Evidence from multiple paradigms. Journal of Child Psychology and Psychiatry and Allied Disciplines, 44(6), 904–913.
Murphy, K. R., & Myors, B. (2004). Statistical power analysis. A simple and general model for traditional and modern hypotheses tests (2nd ed.). Mahwah, NJ: Lawrence Erlbaum Associates.
Oberman, L. M., & Ramachandran, V. M. (2007). The simulating social mind: The role of the mirror neuron system and simulation in the social and communicative deficits of autism spectrum disorders. Psychological Bulletin, 133, 310–327.
Oberman, L. M., Ramachandran, V. S., & Pineda, J. A. (2008). Modulation of mu suppression in children with autism spectrum disorder in response to familiar or unfamiliar stimuli: The mirror neuron hypothesis. Neuropsychologia, 46(5), 1558–1565.
Ozonoff, S. (1997). Casual mechanisms of autism: Unifying perspectives from an information-processing framework. In D. J. Cohen & F. R. Volkmar (Eds.), Handbook of autism and pervasive developmental disorders (pp. 868–879). New York: Wiley.
Ozonoff, S., Strayer, D. L., McMahon, W. M., & Filloux, F. (1994). Executive function abilities in autism and Tourette syndrome: An information processing approach. Journal of Child Psychology and Psychiatry and Allied Disciplines, 35(6), 1015–1132.
Passingham, R. (1995). Frontal lobes and voluntary action. Oxford: Oxford University Press.
Piazza, M., Fumarola, A., Chinello, A., & Melcher, D. (2011). Subitizing reflects visuo-spatial object individuation capacity. Cognition, 121, 147–153.
Platz, T., Kim, I. H., Pintschovious, H., Winter, T., Kieselbach, A., Villringer, K., et al. (2000). Multimodal EEG analysis in man suggests impairment-specific changes in movement-related electric brain activity after stroke. Brain, 123(12), 2475–2490.
Pless, M., Carlsson, M., Sundelin, C., & Persson, K. (2001). Pre-school children with developmental co-ordination disorder: Self-perceived competence and group motor skill intervention. Acta Paediatrica, 90(5), 532–538.
Posner, M. I. (1980). Orienting of attention. Quarterly Journal of Experimental Medicine, 32, 3–25.
Praamstra, P., Schmitz, F., Freund, H. J., & Schnitzler, A. (1999). Magneto-encephalographic correlates of the lateralized readiness potential. Cognitive Brain Research, 8(2), 77–85.
Provost, B., Lopez, B. R., & Heimerl, S. (2007). A comparison of motor delays in young children: Autism spectrum disorder, developmental delay, and developmental concerns. Journal of Autism and Developmental Disorders, 37, 321–328.
Ramachandran, V. S., & Oberman, L. M. (2006). Broken mirrors: A theory of autism. Scientific American, 295(5), 62–69.
Rizzolatti, G., & Craighero, L. (2004). The mirror-neuron system. Annual Review Neuroscience, 27, 169–192.
Rowland, L. P., & Pedley, T. A. (2010). Meritt’s neurology (12th ed.). Philadelphia, PA: Lippincot Williams and Wilkins.
Shallice, T., & Burgess, P. W. (1991). Deficits in strategy application following frontal lobe damage in man. Brain, 114, 727–741.
Smith, S. E., & Chatterjee, A. (2008). Visuospatial attention in children. Archives of Neurology, 65, 1284–1288.
Sokhadze, E., Baruth, J., Tasman, A., Mansoor, M., Ramaswamy, R., Sears, L., et al. (2010). Low-frequency repetitive transcranial magnetic stimulation (rTMS) affects event-related potential measures of novelty processing in autism. Appied Psychophysiology and Biofeedback, 35(2), 147–161.
Sokhadze, E. M., El-Baz, A., Baruth, J., Mathai, G., Sears, L., & Casanova, M. F. (2009). Effect of a low-frequency repetitive transcranial magnetic stimulation (rTMS) on gamma frequency oscillations and event-related potentials during processing of illusory figures in autism. Journal of Autism and Developmental Disorders, 39(4), 619–634.
Spatt, J., & Goldenberg, G. (1997). Speed of motor execution and apraxia. Journal of Clinical and Experimental Neuropsychology, 19, 850–856.
Stieglitz Ham, H., Bartolo, A., Corley, M., Rajendran, G., Szabo, A., & Swanson, S. (2011). Exploring the relationship between gestural recognition and imitation: Evidence of dyspraxia in autism spectrum disorders. Journal of Autism and Developmental Disorders, 41(1), 1–12.
Sutera, S., Pandey, J., Esser, E. L., Rosenthal, M. A., Wilson, L. B., Barton, M., et al. (2007). Predictors of optimal outcome in toddlers diagnosed with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37(1), 98–107.
Ulrich, R., Leuthold, W., & Sommer, W. (1998). Motor programming of response force and movement direction. Psychophysiology, 35, 721–728.
Van Waevelde, H., Oostra, A., Dewitte, G., Van Den Broeck, C., & Jongmans, M. J. (2010). Stability of motor problems in young children with or at risk of autism spectrum disorder, ADHD, and or developmental coordination disorder. Developmental Medicine and Child Neurology, 52(8), e174–e178.
Wang, L., Mottron, L., Peng, D., Berthiaume, C., & Dawson, M. (2007). Local bias and local-to-global interference without global deficit: A robust finding in autism under various conditions of attention, exposure of attention, exposure time, and visual angle. Cognitive Neuropsychology, 24(5), 550–574.
Wascher, E., Verleger, R., Vieregge, P., Jaskowski, P., Koch, S., & Kompf, D. (1997). Responses to cued signals in Parkinson’s disease. Distinguishing between disorders of cognition and of activation. Brain, 120(8), 1355–1375.
Wechsler, D. (2003). Wechsler intelligence scale for children (4th ed.). San Antonio, TX: Harcourt Assessment Inc.
Weimer, A. K., Schatz, A., Lincoln, A., Ballantyne, A. O., & Trauner, D. A. (2001). “Motor” impairment in Asperger syndrome: Evidence for a deficit in propioception. Journal of Developmental and Behavioral Pediatrics, 22(2), 92–101.
Williams, J., Whiten, A., Suddendorf, T., & Perrett, D. (2001). Imitation, mirror neurons, and autism. Neuroscience and Biobehavioral Reviews, 25, 577–596.
Zikopoulos, B., & Barbas, H. (2010). Changes in prefrontal axons may disrupt the network in autism. The Journal of Neuroscience, 30(44), 14595–14609.
Acknowledgments
The study was partially supported by National Institutes of Health Eureka R01 Grant MH86784 to Manuel F. Casanova and by a pilot research grant from Autism Research Institute (San Diego, CA) to Estate M. Sokhadze.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sokhadze, E.M., Tasman, A., Sokhadze, G.E. et al. Behavioral, Cognitive, and Motor Preparation Deficits in a Visual Cued Spatial Attention Task in Autism Spectrum Disorder. Appl Psychophysiol Biofeedback 41, 81–92 (2016). https://doi.org/10.1007/s10484-015-9313-x
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10484-015-9313-x