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Visual Motion Processing and Visual Sensorimotor Control in Autism

  • Yukari Takarae (a1), Beatriz Luna (a2) (a3), Nancy J. Minshew (a2) (a4) and John A. Sweeney (a1) (a5)

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)

Copyright

Corresponding author

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

References

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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.
Anstis, S., Verstraten, F.A., Mather, G. (1998). The motion aftereffect. Trends in Cognitive Science, 2(3), 111117.
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.
Behrmann, M., Thomas, C., Humphreys, K. (2006). Seeing it differently: Visual processing in autism. Trends in Cognitive Science, 10(6), 258264.
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.
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.
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.
Bertone, A., Mottron, L., Jelenic, P., Faubert, J. (2003). Motion perception in autism: A “complex” issue. Journal of Cognitive Neuroscience, 15(2), 218225.
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.
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.
Burke, M.R., Barnes, G.R. (2008). Brain and behavior: A task-dependent eye movement study. Cerebral Cortex, 18(1), 126135.
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.
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.
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.
Cox, R.W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162173.
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.
Dakin, S., Frith, U. (2005). Vagaries of visual perception in autism. Neuron, 48(3), 497507.
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.
Donahue, M.J., Near, J., Blicher, J.U., Jezzard, P. (2011). Baseline GABA concentration and fMRI response. Neuroimage, 53(2), 392398.
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.
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.
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.
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.
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.
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.
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.
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.
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].
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.
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.
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.
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.
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.
Koldewyn, K., Whitney, D., Rivera, S.M. (2010). The psychophysics of visual motion and global form processing in autism. Brain, 133(Pt 2), 599610.
Koldewyn, K., Whitney, D., Rivera, S.M. (2011). Neural correlates of coherent and biological motion perception in autism. Developmental Science, 14(5), 10751088.
Krekelberg, B., Boynton, G.M., van Wezel, R.J. (2006). Adaptation: From single cells to BOLD signals. Trends in Neuroscience, 29(5), 250256.
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.
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.
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.
Manning, C., Aagten-Murphy, D., Pellicano, E. (2012). The development of speed discrimination abilities. Vision Research, 70, 2733.
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.
Milne, E., Swettenham, J., Campbell, R. (2005). Motion perception and autistic spectrum disorder: A review. Current Psychology of Cognition, 23(1), 336.
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.
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.
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.
O'Hearn, K., Asato, M., Ordaz, S., Luna, B. (2008). Neurodevelopment and executive function in autism. Developmental Psychopathology, 20(4), 11031132.
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.
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.
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.
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.
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.
Spence, S.J., Schneider, M.T. (2009). The role of epilepsy and epileptiform EEGs in autism spectrum disorders. Pediatric Research, 65(6), 599606.
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.
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.
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.
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.
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.
Talairach, J., Tournoux, P. (1998). Co-planar stereotaxic atlas of the human brain. New York: Thieme Medical Publishers.
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.
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.
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.
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.
Van Wezel, R.J., Britten, K.H. (2002). Motion adaptation in area MT. Journal of Neurophysiology, 88(6), 34693476.
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.
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.

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Visual Motion Processing and Visual Sensorimotor Control in Autism

  • Yukari Takarae (a1), Beatriz Luna (a2) (a3), Nancy J. Minshew (a2) (a4) and John A. Sweeney (a1) (a5)

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