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Visual Motion Processing and Visual Sensorimotor Control in Autism

Published online by Cambridge University Press:  23 December 2013

Yukari Takarae*
Affiliation:
Center for Autism and Developmental Disabilities, Department of Psychiatry, University of Texas Southwestern, Dallas, Texas
Beatriz Luna
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, Pennsylvania Department of Psychology, University of Pittsburgh, Pittsburgh, Pennsylvania
Nancy J. Minshew
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, Pennsylvania Department of Neurology, University of Pittsburgh, Pittsburgh, Pennsylvania
John A. Sweeney
Affiliation:
Center for Autism and Developmental Disabilities, Department of Psychiatry, University of Texas Southwestern, Dallas, Texas Department of Pediatrics, University of Texas Southwestern, Dallas, Texas
*
Correspondence and reprint requests to: Yukari Takarae, Ph.D., Department of Psychiatry, Center for Autism and Developmental Disabilities, University of Texas Southwestern, 5323 Harry Hines Blvd MC9086, Dallas TX 75390. E-mail: yukari.takarae@southwestern.edu

Abstract

Impairments in visual motion perception and use of visual motion information to guide behavior have been reported in autism, but the brain alterations underlying these abnormalities are not well characterized. We performed functional magnetic resonance imaging (fMRI) studies to investigate neural correlates of impairments related to visual motion processing. Sixteen high-functioning individuals with autism and 14 age and IQ-matched typically developing individuals completed two fMRI tasks using passive viewing to examine bottom–up responses to visual motion and visual pursuit tracking to assess top–down modulation of visual motion processing during sensorimotor control. The autism group showed greater activation and faster hemodynamic decay in V5 during the passive viewing task and reduced frontal and V5 activation during visual pursuit. The observations of increased V5 activation and its faster decay during passive viewing suggest alterations in local V5 circuitries that may be associated with reduced GABAergic tone and inhibitory modulation. Reduced frontal and V5 activation during active pursuit suggest reduced top–down modulation of sensory processing. These results suggest that both local intrinsic abnormalities in V5 and more widely distributed network level abnormalities are associated with visual motion processing in autism. (JINS, 2014, 20, 113–122)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2014 

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References

Annaz, D., Remington, A., Milne, E., Coleman, M., Campbell, R., Thomas, M.S., Swettenham, J. (2010). Development of motion processing in children with autism. Developmental Science, 13(6), 826838.Google Scholar
Anstis, S., Verstraten, F.A., Mather, G. (1998). The motion aftereffect. Trends in Cognitive Science, 2(3), 111117.Google Scholar
Bair, W., Cavanaugh, J.R., Movshon, J.A. (2003). Time course and time-distance relationships for surround suppression in macaque V1 neurons. Journal of Neuroscience, 23(20), 76907701.Google Scholar
Behrmann, M., Thomas, C., Humphreys, K. (2006). Seeing it differently: Visual processing in autism. Trends in Cognitive Science, 10(6), 258264.Google Scholar
Berman, R.A., Colby, C.L. (2002). Auditory and visual attention modulate motion processing in area MT+. Brain Research Cognitive Brain Research, 14(1), 6474.Google Scholar
Berman, R.A., Colby, C.L., Genovese, C.R., Voyvodic, J.T., Luna, B., Thulborn, K.R., Sweeney, J.A. (1999). Cortical networks subserving pursuit and saccadic eye movements in humans: An FMRI study. Human Brain Mapping, 8(4), 209225.Google Scholar
Bertone, A., Faubert, J. (2006). Demonstrations of decreased sensitivity to complex motion information not enough to propose an autism-specific neural etiology. Journal of Autism and Developmental Disorders, 36(1), 5564.Google Scholar
Bertone, A., Mottron, L., Jelenic, P., Faubert, J. (2003). Motion perception in autism: A “complex” issue. Journal of Cognitive Neuroscience, 15(2), 218225.CrossRefGoogle ScholarPubMed
Blatt, G.J., Fitzgerald, C.M., Guptill, J.T., Booker, A.B., Kemper, T.L., Bauman, M.L. (2001). Density and distribution of hippocampal neurotransmitter receptors in autism: An autoradiographic study. Journal of Autism and Developmental Disorders, 31(6), 537543.Google Scholar
Brieber, S., Herpertz-Dahlmann, B., Fink, G.R., Kamp-Becker, I., Remschmidt, H., Konrad, K. (2010). Coherent motion processing in autism spectrum disorder (ASD): An fMRI study. Neuropsychologia, 48(6), 16441651.Google Scholar
Burke, M.R., Barnes, G.R. (2008). Brain and behavior: A task-dependent eye movement study. Cerebral Cortex, 18(1), 126135.Google Scholar
Castelo-Branco, M., Kozak, L.R., Formisano, E., Teixeira, J., Xavier, J., Goebel, R. (2009). Type of featural attention differentially modulates hMT+ responses to illusory motion aftereffects. Journal of Neurophysiology, 102(5), 30163025.Google Scholar
Coghlan, S., Horder, J., Inkster, B., Mendez, M.A., Murphy, D.G., Nutt, D.J. (2012). GABA system dysfunction in autism and related disorders: From synapse to symptoms. Neuroscience Biobehavioral Review, 36(9), 20442055.Google Scholar
Collins, A.L., Ma, D., Whitehead, P.L., Martin, E.R., Wright, H.H., Abramson, R.K., Pericak-Vance, M.A. (2006). Investigation of autism and GABA receptor subunit genes in multiple ethnic groups. Neurogenetics, 7(3), 167174.Google Scholar
Cox, R.W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162173.Google Scholar
Culham, J.C., Dukelow, S.P., Vilis, T., Hassard, F.A., Gati, J.S., Menon, R.S., Goodale, M.A. (1999). Recovery of fMRI activation in motion area MT following storage of the motion aftereffect. Journal of Neurophysiology, 81(1), 388393.Google Scholar
Dakin, S., Frith, U. (2005). Vagaries of visual perception in autism. Neuron, 48(3), 497507.CrossRefGoogle ScholarPubMed
Dieterich, M., Muller-Schunk, S., Stephan, T., Bense, S., Seelos, K., Yousry, T.A. (2009). Functional magnetic resonance imaging activations of cortical eye fields during saccades, smooth pursuit, and optokinetic nystagmus. Annals of New York Academy of Science, 1164, 282292.CrossRefGoogle ScholarPubMed
Donahue, M.J., Near, J., Blicher, J.U., Jezzard, P. (2011). Baseline GABA concentration and fMRI response. Neuroimage, 53(2), 392398.Google Scholar
Eddy, W., Fitzgerald, M., Genovese, C., Mockus, A., Noll, D. (1996). Functional Imaging Analysis Software – Computational Olio. In A. Prat (Ed.), COMPSTAT (pp. 3949). Physica-Verlag HD.CrossRefGoogle Scholar
Fatemi, S.H., Halt, A.R., Stary, J.M., Kanodia, R., Schulz, S.C., Realmuto, G.R. (2002). Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices. Biological Psychiatry, 52(8), 805810.Google Scholar
Freitag, C.M., Konrad, C., Haberlen, M., Kleser, C., von Gontard, A., Reith, W., Krick, C. (2008). Perception of biological motion in autism spectrum disorders. Neuropsychologia, 46(5), 14801494.CrossRefGoogle ScholarPubMed
Freitag, P., Greenlee, M.W., Lacina, T., Scheffler, K., Radu, E.W. (1998). Effect of eye movements on the magnitude of functional magnetic resonance imaging responses in extrastriate cortex during visual motion perception. Experimental Brain Research, 119(4), 409414.Google Scholar
Gibbons, R.D., Lazar, N.A., Bhaumik, D.K., Sclove, S.L., Chen, H.Y., Thulborn, K.R., Patterson, D. (2004). Estimation and classification of fMRI hemodynamic response patterns. Neuroimage, 22(2), 804814.Google Scholar
Hadad, B.S., Maurer, D., Lewis, T.L. (2011). Long trajectory for the development of sensitivity to global and biological motion. Developmental Science, 14(6), 13301339.Google Scholar
He, S., Cohen, E.R., Hu, X. (1998). Close correlation between activity in brain area MT/V5 and the perception of a visual motion aftereffect. Current Biology, 8(22), 12151218.Google Scholar
Heeger, D.J., Boynton, G.M., Demb, J.B., Seidemann, E., Newsome, W.T. (1999). Motion opponency in visual cortex. Journal of Neuroscience, 19(16), 71627174.Google Scholar
Heinen, K., Feredoes, E., Weiskopf, N., Ruff, C.C., Driver, J. (2013). Direct evidence for attention-dependent influences of the frontal eye-fields on feature-responsive visual cortex. Cerebral Cortex [Epub ahead of print].Google Scholar
Jamain, S., Betancur, C., Quach, H., Philippe, A., Fellous, M., Giros, B., Bourgeron, T. (2002). Linkage and association of the glutamate receptor 6 gene with autism. Molecular Psychiatry, 7(3), 302310.Google Scholar
Jones, C.R., Swettenham, J., Charman, T., Marsden, A.J., Tregay, J., Baird, G., Happe, F. (2011). No evidence for a fundamental visual motion processing deficit in adolescents with autism spectrum disorders. Autism Research, 4(5), 347357.CrossRefGoogle ScholarPubMed
Kaiser, M.D., Shiffrar, M. (2009). The visual perception of motion by observers with autism spectrum disorders: A review and synthesis. Psychonomic Bulletin & Review, 16(5), 761777.CrossRefGoogle ScholarPubMed
Keita, L., Mottron, L., Dawson, M., Bertone, A. (2011). Atypical lateral connectivity: A neural basis for altered visuospatial processing in autism. Biological Psychiatry, 70(9), 806811.Google Scholar
Kimmig, H., Ohlendorf, S., Speck, O., Sprenger, A., Rutschmann, R.M., Haller, S., Greenlee, M.W. (2008). fMRI evidence for sensorimotor transformations in human cortex during smooth pursuit eye movements. Neuropsychologia, 46(8), 22032213.CrossRefGoogle ScholarPubMed
Koldewyn, K., Whitney, D., Rivera, S.M. (2010). The psychophysics of visual motion and global form processing in autism. Brain, 133(Pt 2), 599610.CrossRefGoogle ScholarPubMed
Koldewyn, K., Whitney, D., Rivera, S.M. (2011). Neural correlates of coherent and biological motion perception in autism. Developmental Science, 14(5), 10751088.Google Scholar
Krekelberg, B., Boynton, G.M., van Wezel, R.J. (2006). Adaptation: From single cells to BOLD signals. Trends in Neuroscience, 29(5), 250256.Google Scholar
Lazar, N.A, Luna, B., Sweeney, J.A., Eddy, W.F. (2002). Combining brains: a survey of methods for statistical pooling of information. Neuroimage, 16(2), 538550.Google Scholar
Lord, C., Risi, S., Lambrecht, L., Cook, E.H. Jr., Leventhal, B.L., DiLavore, P.C., 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(3), 205223.CrossRefGoogle ScholarPubMed
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(5), 659685.CrossRefGoogle ScholarPubMed
Manning, C., Aagten-Murphy, D., Pellicano, E. (2012). The development of speed discrimination abilities. Vision Research, 70, 2733.Google Scholar
Merriam, E.P., Colby, C.L., Thulborn, K.R., Luna, B., Olson, C.R., Sweeney, J.A. (2001). Stimulus-response incompatibility activates cortex proximate to three eye fields. Neuroimage, 13(5), 794800.Google Scholar
Milne, E., Swettenham, J., Campbell, R. (2005). Motion perception and autistic spectrum disorder: A review. Current Psychology of Cognition, 23(1), 336.Google Scholar
Milne, E., Swettenham, J., Hansen, P., Campbell, R., Jeffries, H., Plaisted, K. (2002). High motion coherence thresholds in children with autism. Journal of Child Psychology and Psychiatry, 43(2), 255263.Google Scholar
Mosconi, M.W., Takarae, Y., Sweeney, J.A. (2011). Motor functioning and dyspraxia in Autism Spectrum Disorders. In D. G. Amaral, G. Dawson, D. H. Geshwind (Eds.), Autism spectrum disorders (pp. 355380). New York, NY: Oxford University Press.Google Scholar
Muthukumaraswamy, S.D., Evans, C.J., Edden, R.A., Wise, R.G., Singh, K.D. (2012). Individual variability in the shape and amplitude of the BOLD-HRF correlates with endogenous GABAergic inhibition. Human Brain Mapping, 33(2), 455465.CrossRefGoogle ScholarPubMed
O'Hearn, K., Asato, M., Ordaz, S., Luna, B. (2008). Neurodevelopment and executive function in autism. Developmental Psychopathology, 20(4), 11031132.Google Scholar
Oblak, A., Gibbs, T.T., Blatt, G.J. (2009). Decreased GABA(A) receptors and benzodiazepine binding sites in the anterior cingulate cortex in autism. Autism Research, 2, 205219.Google Scholar
Ruff, C.C., Bestmann, S., Blankenburg, F., Bjoertomt, O., Josephs, O., Weiskopf, N., Driver, J. (2008). Distinct causal influences of parietal versus frontal areas on human visual cortex: Evidence from concurrent TMS-fMRI. Cerebral Cortex, 18(4), 817827.Google Scholar
Ruff, C.C., Blankenburg, F., Bjoertomt, O., Bestmann, S., Freeman, E., Haynes, J.D., Driver, J. (2006). Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Current Biology, 16(15), 14791488.Google Scholar
Samson, F., Mottron, L., Soulieres, I., Zeffiro, T.A. (2012). Enhanced visual functioning in autism: An ALE meta-analysis. Human Brain Mapping, 33(7), 15531581.Google Scholar
Snijders, T.M., Milivojevic, B., Kemner, C. (2013). Atypical excitation-inhibition balance in autism captured by the gamma response to contextual modulation. Neuroimage: Clinical, 3, 6572.CrossRefGoogle ScholarPubMed
Spence, S.J., Schneider, M.T. (2009). The role of epilepsy and epileptiform EEGs in autism spectrum disorders. Pediatric Research, 65(6), 599606.Google Scholar
Spencer, J., O'Brien, J., Riggs, K., Braddick, O., Atkinson, J., Wattam-Bell, J. (2000). Motion processing in autism: Evidence for a dorsal stream deficiency. Neuroreport, 11(12), 27652767.Google Scholar
Spiegel, D.P., Hansen, B.C., Byblow, W.D., Thompson, B. (2012). Anodal transcranial direct current stimulation reduces psychophysically measured surround suppression in the human visual cortex. PLoS One, 7(5), e36220.Google Scholar
Takarae, Y., Luna, B., Minshew, N.J., Sweeney, J.A. (2008). Patterns of visual sensory and sensorimotor abnormalities in autism vary in relation to history of early language delay. Journal of the International Neuropsychological Society, 14(6), 980989.Google Scholar
Takarae, Y., Minshew, N.J., Luna, B., Krisky, C.M., Sweeney, J.A. (2004). Pursuit eye movement deficits in autism. Brain, 127(Pt 12), 25842594.CrossRefGoogle ScholarPubMed
Takarae, Y., Minshew, N.J., Luna, B., Sweeney, J.A. (2007). Atypical involvement of frontostriatal systems during sensorimotor control in autism. Psychiatry Research: Neuroimaging, 156(2), 117127.Google Scholar
Talairach, J., Tournoux, P. (1998). Co-planar stereotaxic atlas of the human brain. New York: Thieme Medical Publishers.Google Scholar
Thiele, A., Distler, C., Korbmacher, H., Hoffmann, K.P. (2004). Contribution of inhibitory mechanisms to direction selectivity and response normalization in macaque middle temporal area. Proceeding of National Academy of Science of the United States of America, 101(26), 98109815.Google Scholar
Tootell, R.B., Reppas, J.B., Dale, A.M., Look, R.B., Sereno, M.I., Malach, R., Rosen, B.R. (1995). Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature, 375(6527), 139141.Google Scholar
Tsermentseli, S., O'Brien, J.M., Spencer, J.V. (2008). Comparison of form and motion coherence processing in autistic spectrum disorders and dyslexia. Journal of Autism and Developmental Disorders, 38(7), 12011210.Google Scholar
van den Boomen, C., van der Smagt, M.J., Kemner, C. (2012). Keep your eyes on development: The behavioral and neurophysiological development of visual mechanisms underlying form processing. Frontiers in Psychiatry, 3, 16.Google Scholar
Van Wezel, R.J., Britten, K.H. (2002). Motion adaptation in area MT. Journal of Neurophysiology, 88(6), 34693476.Google Scholar
Williams, D.L., Goldstein, G., Minshew, N.J. (2006). Neuropsychologic functioning in children with autism: further evidence for disordered complex information-processing. Child Neuropsychology, 12(4–5), 279298.Google Scholar
Yip, J., Soghomonian, J.J., Blatt, G.J. (2007). Decreased GAD67 mRNA levels in cerebellar Purkinje cells in autism: Pathophysiological implications. Acta Neuropathologica, 113(5), 559568.Google Scholar
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