Journal of Autism and Developmental Disorders

, Volume 37, Issue 7, pp 1289–1309 | Cite as

Eye Movement and Visual Search: Are There Elementary Abnormalities in Autism?

  • Laurie A. Brenner
  • Katherine C. Turner
  • Ralph-Axel Müller
Original Paper


Although atypical eye gaze is commonly observed in autism, little is known about underlying oculomotor abnormalities. Our review of visual search and oculomotor systems in the healthy brain suggests that relevant networks may be partially impaired in autism, given regional abnormalities known from neuroimaging. However, direct oculomotor evidence for autism remains limited. This gap is critical since oculomotor abnormalities might play a causal role in functions known to be impaired in autism, such as imitation and joint attention. We integrate our oculomotor review into a developmental approach to language impairment related to nonverbal prerequisites. Oculomotor abnormalities may play a role as a sensorimotor defect at the root of impairments in later developing functional systems, ultimately resulting in sociocommunicative deficits.


Autism Eye movement Visual search Joint attention Language 



This review was supported by NIH grant R01-DC6155 (LAB, KCT, RAM) and R01-NS43999 (RAM).


  1. Akshoomoff, N., Courchesne, E., & Townsend, J. (1997). Attention coordination and anticipatory control. International Review of Neurobiology, 41, 575–598.PubMedGoogle Scholar
  2. Akshoomoff, N., Pierce, K., & Courchesne, E. (2002). The neurobiological basis of autism from a developmental perspective. Development and Psychopathology, 14(3), 613–634.PubMedCrossRefGoogle Scholar
  3. Apicella, P., Scarnati, E., Ljungberg, T., & Schultz, W. (1992). Neuronal activity in monkey striatum related to the expectation of predictable environmental events. Journal of Neurophysiology, 68, 945–960.PubMedGoogle Scholar
  4. Bacon, A. L., Fein, D., Morris, R., Waterhouse, L., & Allen, D. (1998). The responses of autistic children to the distress of others. Journal of Autism and Developmental Disorders, 28(2), 129–142.PubMedCrossRefGoogle Scholar
  5. Bailey, A., Luthert, P., Dean, A., Harding, B., Janota, I., Montgomery, M., et al. (1998). A clinicopathological study of autism. Brain, 121(Pt 5), 889–905.PubMedCrossRefGoogle Scholar
  6. Baird, G., Charman, T., Baron-Cohen, S., Cox, A., Swettenham, J., Wheelwright, S., et al. (2000). A screening instrument for autism at 18 months of age: a 6-year follow-up study. Journal of American Academy of Child and Adolescent Psychiatry, 39(6), 694–702.CrossRefGoogle Scholar
  7. Baltaxe, C. A., & Simmons, J. Q. (1975). Language in childhood psychosis: a review. Journal of Speech and Hearing Disorders, 40(4), 439–458.PubMedGoogle Scholar
  8. Barnea-Goraly, N., Kwon, H., Menon, V., Eliez, S., Lotspeich, L., & Reiss, A. L. (2004). White matter structure in autism: preliminary evidence from diffusion tensor imaging. Biol Psychiatry, 55(3), 323–326.PubMedCrossRefGoogle Scholar
  9. Baron-Cohen, S., Ring, H. A., Wheelwright, S., Bullmore, E. T., Brammer, M. J., Simmons, A., et al. (1999). Social intelligence in the normal and autistic brain: An fMRI study. European Journal of Neuroscience, 11(6), 1891–1898.PubMedCrossRefGoogle Scholar
  10. Belmonte, M. K., & Yurgelun-Todd, D. A. (2003). Functional anatomy of impaired selective attention and compensatory processing in autism. Cogn Brain Res, 17(3), 651–664.CrossRefGoogle Scholar
  11. Berman, R., Colby, C., Genovese, C., Voyvodic, J., Luna, B., Thulborn, K., et al. (1999). Cortical networks subserving pursuit and saccadic eye movements in humans: an fMRI study. Human Brain Mapping, 8(4), 209–225.PubMedCrossRefGoogle Scholar
  12. Binkofski, F., Amunts, K., Stephan, K. M., Posse, S., Schormann, T., Freund, H. J., et al. (2000). Broca’s region subserves imagery of motion: a combined cytoarchitectonic and fMRI study. Human Brain Mapping, 11(4), 273–285.PubMedCrossRefGoogle Scholar
  13. Brambilla, P., Hardan, A., di Nemi, S. U., Perez, J., Soares, J. C., & Barale, F. (2003). Brain anatomy and development in autism: review of structural MRI studies. Brain Research Bulletin, 61(6), 557–569.PubMedCrossRefGoogle Scholar
  14. Brandt, S., Ploner, C., Meyer, B.-U., Leistner, S., & Villringer, A. (1998). Effects of repetitive transcranial magnetic stimulation over dorsolateral prefrontal and posterior parietal cortex on memory-guided saccades. Experimental Brain Research, 118, 197–204.CrossRefGoogle Scholar
  15. Brooks, R., & Meltzoff, A. N. (2005). The development of gaze following and its relation to language. Developmental Science, 8(6), 535–543.PubMedCrossRefGoogle Scholar
  16. Buccino, G., Binkofski, F., Fink, G. R., Fadiga, L., Fogassi, L., Gallese, V., et al. (2001). Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. European Journal of Neuroscience, 13(2), 400–404.PubMedCrossRefGoogle Scholar
  17. Buccino, G., Binkofski, F., & Riggio, L. (2004). The mirror neuron system and action recognition. Brain and Language, 89(2), 370–376.PubMedCrossRefGoogle Scholar
  18. Burack, J. (1994). Selective attention deficits in persons with autism: preliminary evidence of an inefficient attentional lens. Journal of Abnormal Psychology, 103, 535–543.PubMedCrossRefGoogle Scholar
  19. Camaioni, L., Perucchini, P., Muratori, F., Parrini, B., & Cesari, A. (2003). The communicative use of pointing in autism: developmental profile and factors related to change. European Psychiatry, 18(1), 6–12.PubMedCrossRefGoogle Scholar
  20. Carpenter, M., Nagell, K., & Tomasello, M. (1998). Social cognition, joint attention, and communicative competence from 9 to 15 months of age. Monographs of the Society for Research in Child Development, 63(4), i-vi, 1–143.Google Scholar
  21. Carpenter, M., Pennington, B. F., & Rogers, S. J. (2002). Interrelations among social-cognitive skills in young children with autism. Journal of Autism and Developmental Disorders, 32(2), 91–106.PubMedCrossRefGoogle Scholar
  22. Carper, R. A., & Courchesne, E. (2005). Localized enlargement of the frontal cortex in early autism. Biological Psychiatry, 57(2), 126–133.PubMedCrossRefGoogle Scholar
  23. Carper, R. A., Moses, P., Tigue, Z. D., & Courchesne, E. (2002). Cerebral lobes in autism: early hyperplasia and abnormal age effects. Neuroimage, 16(4), 1038–1051.PubMedCrossRefGoogle Scholar
  24. Castelli, F., Frith, C., Happe, F., & Frith, U. (2002). Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain, 125(Pt 8), 1839–1849.PubMedCrossRefGoogle Scholar
  25. Charman, T. (2003). Why is joint attention a pivotal skill in autism? Philosophical Transactions of the Royal Society of London. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, 358(1430), 315–324.PubMedCrossRefGoogle Scholar
  26. Ciesielski, K. T., Harris, R. J., Hart, B. L., & Pabst, H. F. (1997). Cerebellar hypoplasia and frontal lobe cognitive deficits in disorders of early childhood. Neuropsychologia, 35(5), 643–655.PubMedCrossRefGoogle Scholar
  27. Colombo, J. (2001). The development of visual attention in infancy. Annual Review of Psychology, 52, 337–367.PubMedCrossRefGoogle Scholar
  28. Corbetta, M., Kincade, M., Ollinger, J., McAvoy, M., & Shulman, G. (2000). Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nature Neuroscience, 3(3), 292–297.PubMedCrossRefGoogle Scholar
  29. Cornelissen, F., Kimmig, H., Schira, M., Rutschmann, R., Maguire, R., Broerse, A., et al. (2002). Event-related fMRI responses in the human frontal eye fields in a randomized pro- and antisaccade task. Experimental Brain Research, 145, 270–274.CrossRefGoogle Scholar
  30. Courchesne, E., Karns, C. M., Davis, H. R., Ziccardi, R., Carper, R. A., Tigue, Z. D., et al. (2001). Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology, 57(2), 245–254.PubMedGoogle Scholar
  31. Courchesne, E., & Pierce, K. (2005). Brain overgrowth in autism during a critical time in development: implications for frontal pyramidal neuron and interneuron development and connectivity. International Journal of Developmental Neuroscience, 23(2–3), 153–170.PubMedCrossRefGoogle Scholar
  32. Courchesne, E., Press, G. A., & Yeung-Courchesne, R. (1993). Parietal lobe abnormalities detected with MR in patients with infantile autism. AJR. American Journal of Roentgenology, 160(2), 387–393.PubMedGoogle Scholar
  33. Courchesne, E., Townsend, J., Akshoomoff, N. A., Saitoh, O., Yeung-Courchesne, R., Lincoln, A. J., et al. (1994). Impairment in shifting attention in autistic and cerebellar patients. Behavioral Neuroscience, 108(5), 848–865.PubMedCrossRefGoogle Scholar
  34. Courchesne, E., Yeung-Courchesne, R., Press, G. A., Hesselink, J. R., & Jernigan, T. L. (1988). Hypoplasia of cerebellar vermal lobules VI and VII in autism. New England Journal of Medicine, 318(21), 1349–1354.PubMedCrossRefGoogle Scholar
  35. Csibra, G., Tucker, L. A., & Johnson, M. H. (1998). Neural correlates of saccade planning in infants: a high-density ERP study. International Journal of Psychophysiology, 29(2), 201–215.PubMedCrossRefGoogle Scholar
  36. Damasio, A. R., & Maurer, R. G. (1978). A neurological model for childhood autism. Archives of Neurology, 35, 777–786.PubMedGoogle Scholar
  37. Dawson, G., Meltzoff, A. N., Osterling, J., Rinaldi, J., & Brown, E. (1998). Children with autism fail to orient to naturally occurring social stimuli. Journal of Autism and Developmental Disorders, 28(6), 479–485.PubMedCrossRefGoogle Scholar
  38. Delis, D., Kaplan, E., & Kramer, J. (2001). Delis-Kaplan executive function system. San Antonio, TX: The Psychological Corporation.Google Scholar
  39. Desimone, R., & Duncan, J. (1995). Neural mechanisms of selective visual attention. Annual Review of Neuroscience, 18, 193–222.PubMedCrossRefGoogle Scholar
  40. DeSouza, J., Menon, R., & Everling, S. (2003). Preparatory set associated with pro-saccades and anti-saccades in humans investigated with event-related fMRI. Journal of Neurophysiology, 89, 1016–1023.PubMedCrossRefGoogle Scholar
  41. Deubel, H., & Schneider, W. (1996). Saccade target selection and object recognition: evidence for a common attentional mechanism. Vision Research, 36, 1827–1837.PubMedCrossRefGoogle Scholar
  42. Donner, T., Kettermann, A., Diesch, E., Ostendorf, F., Villringer, A., & Brandt, S. (2002). Visual feature and conjunction searches of equal difficulty engage only partially overlapping frontoparietal networks. Neuroimage, 15, 16–25.PubMedCrossRefGoogle Scholar
  43. Duncan, J., & Humphreys, G. (1989). Visual search and stimulus similarity. Psychological Review, 96, 433–458.PubMedCrossRefGoogle Scholar
  44. Ek, U., Fernell, E., & Jacobson, L. (2005). Cognitive and behavioural characteristics in blind children with bilateral optic nerve hypoplasia. Acta Paediatr, 94(10), 1421–1426.PubMedCrossRefGoogle Scholar
  45. Elbert, T., Heim, S., & Rockstroh, B. (2001). Neural plasticity and development. In C. A. Nelson & M. Luciana (Eds.), Handbook of developmental cognitive neuroscience (pp. 191–202). Cambridge (MA): MIT Press.Google Scholar
  46. Elbert, T., Pantev, C., Wienbruch, C., Rockstroh, B., & Taub, E. (1995). Increased cortical representation of the fingers of the left hand in string players. Science, 270, 305–307.PubMedCrossRefGoogle Scholar
  47. Fatemi, S. H., Halt, A. R., Realmuto, G., Earle, J., Kist, D. A., Thuras, P., et al. (2002). Purkinje cell size is reduced in cerebellum of patients with autism. Cellular and Molecular Neurobiology, 22(2), 171–175.PubMedCrossRefGoogle Scholar
  48. Ferraina, S., Pare, M., & Wurtz, R. (2002). Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movement. Journal of Neurophysiology, 87, 845–858.PubMedGoogle Scholar
  49. Fincham, J. M., Carter, C. S., van Veen, V., Stenger, V. A., & Anderson, J. R. (2002). Neural mechanisms of planning: a computational analysis using event-related fMRI. Proc Natl Acad Sci USA, 99(5), 3346–3351.PubMedCrossRefGoogle Scholar
  50. Findlay, J., & Gilchrist, I. (2003). Active vision: The physiology of looking and seeing. New York: Oxford University Press.Google Scholar
  51. Frith, U. (1989). Autism: Explaining the enigma. Oxford: Blackwell.Google Scholar
  52. Fukushima, J., Hatta, T., & Fukushima, K. (2000). Development of voluntary control of saccadic eye movements I. Age-related changes in normal children. Brain and Development, 22, 173–180.PubMedCrossRefGoogle Scholar
  53. Garber, H. J., & Ritvo, E. R. (1989). A magnetic resonance imaging study of autism: normal fourth ventricle size and absence of pathology. American Journal of Psychiatry, 146, 532–534.PubMedGoogle Scholar
  54. Gaymard, B., Lynch, J., Ploner, C., Condy, C., & Rivaud-Pechoux, S. (2003). The parieto-collicular pathway: anatomical location and contribution to saccade generation. European Journal of Neuroscience, 17(7), 1518–1526.PubMedCrossRefGoogle Scholar
  55. Gaymard, B., Ploner, C., Rivaud, S., Vermersch, A., & Pierrot-Deseilligny, C. (1998). Cortical control of saccades. Experimental Brain Research, 123, 159–163.CrossRefGoogle Scholar
  56. Gervais, H., Belin, P., Boddaert, N., Leboyer, M., Coez, A., Sfaello, I., et al. (2004). Abnormal cortical voice processing in autism. Nature Neuroscience, 7(8), 801–802.PubMedCrossRefGoogle Scholar
  57. Gitelman, D. R., Parrish, T. B., Friston, K. J., & Mesulam, M. M. (2002). Functional anatomy of visual search: regional segregations within the frontal eye fields and effective connectivity of the superior colliculus. Neuroimage, 15(4), 970–982.PubMedCrossRefGoogle Scholar
  58. Goldberg, M. C., Lasker, A. G., Zee, D. S., Garth, E., Tien, A., & Landa, R. J. (2002). Deficits in the initiation of eye movements in the absence of a visual target in adolescents with high functioning autism. Neuropsychologia, 40(12), 2039–2049.PubMedCrossRefGoogle Scholar
  59. Grosbras, M.-H., Lobel, E., Van de Moortele, P.-F., LeBihan, D., & Berthoz, A. (1999). An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging. Cerebral Cortex, 9, 705–711.PubMedCrossRefGoogle Scholar
  60. Hadjikhani, N., Joseph, R. M., Snyder, J., Chabris, C. F., Clark, J., Steele, S., et al. (2004). Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces. Neuroimage, 22(3), 1141–1150.PubMedCrossRefGoogle Scholar
  61. Haist, F., Adamo, M., Westerfield, M., Courchesne, E., & Townsend, J. (2005). The functional neuroanatomy of spatial attention in autism spectrum disorder. Dev Neuropsychol, 27(3), 425–458.PubMedCrossRefGoogle Scholar
  62. Hanes, D., & Wurtz, R. (2001). Interaction of the frontal eye field and superior colliculus for saccade generation. Journal of Neurophysiology, 85, 804–815.PubMedGoogle Scholar
  63. Happe, F. (1998). Why success is more interesting than failure: understanding assets and deficits in autism. Paper presented at the Society’s London Conference, London.Google Scholar
  64. Harris, N., Courchesne, E., Townsend, J., Carper, R., & Lord, C. (1999). Neuroanatomic contributions to slowed orienting of attention in children with autism. Cognitive Brain Research, 8, 61–71.PubMedCrossRefGoogle Scholar
  65. Hashimoto, T., Tayama, M., Murakawa, K., Yoshimoto, T., Miyazaki, M., Harada, M., et al. (1995). Development of the brainstem and cerebellum in autistic patients. Journal of Autism and Developmental Disorders, 25(1), 1–18.PubMedCrossRefGoogle Scholar
  66. Hayakawa, T., Miyauchi, S., Fujimaki, N., Kato, M., & Yagi, A. (2003). Information flow related to visual search assessed using magnetoencephalography. Cognitive Brain Research, 15(3), 285–295.PubMedCrossRefGoogle Scholar
  67. Hayakawa, T., Nakajima, T., Takagi, M., Fukuhara, N., & Abe, H. (2002). Human cerebellar activation in relation to saccadic eye movements: a functional magnetic resonance imaging study. Opthalmologica, 216, 399–405.Google Scholar
  68. 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(4), 530–540.PubMedCrossRefGoogle Scholar
  69. Hideo, I. (1987). Eye movements in autistic, mentally retarded and normal young children: Simultaneous measurement by an eye camera system for autistic children (ECSA) and an electro-oculography (EOG). RIEEC Report, 36(Feb), 73–81.Google Scholar
  70. Hikosaka, O., Sakamoto, M., & Usui, S. (1983). Visual and oculomotor functions of monkey sustantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. J Neurophysiology, 49, 1268–1284.Google Scholar
  71. Hikosaka, O., Sakamoto, M., & Usui, S. (1989). Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. Journal of Neurophysiology, 61, 814–832.PubMedGoogle Scholar
  72. Hikosaka, O., Takikawa, Y., & Kawagoe, R. (2000). Role of the basal ganglia in the control of purposive saccadic eye movements. Physiological Reviews, 80(3), 953–978.PubMedGoogle Scholar
  73. Howlin, P., Goode, S., Hutton, J., & Rutter, M. (2004). Adult outcome for children with autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 45(2), 212–229.Google Scholar
  74. Hubl, D., Bolte, S., Feineis-Matthews, S., Lanfermann, H., Federspiel, A., Strik, W., et al. (2003). Functional imbalance of visual pathways indicates alternative face processing strategies in autism. Neurology, 61(9), 1232–1237.PubMedGoogle Scholar
  75. Hunt, R., & Ellis, H. (1999). Fundamentals of cognitive psychology (6th ed.). Boston: McGraw-Hill College.Google Scholar
  76. Iacoboni, M., Woods, R. P., Brass, M., Bekkering, H., Mazziotta, J. C., & Rizzolatti, G. (1999). Cortical mechanisms of human imitation. Science, 286(5449), 2526–2528.PubMedCrossRefGoogle Scholar
  77. Johnson, M. H. (1995). The inhibition of automatic saccades in early infancy. Developmental Psychobiology, 28(5), 281–291.PubMedCrossRefGoogle Scholar
  78. Johnson, M. H., Griffin, R., Csibra, G., Halit, H., Farroni, T., de Haan, M., et al. (2005). The emergence of the social brain network: Evidence from typical and atypical development. Developmental Psychobiology, 17(3), 599–619.Google Scholar
  79. Jolliffe, T., & Baron-Cohen, S. (1997). Are people with autism and Asperger syndrome faster than normal on the Embedded Figure Test? Journal of Child Psychology and Psychiatry and Allied Disciplines, 38(5), 527–534.Google Scholar
  80. Juan, C., Shorter-Jacobi, S., & Schall, J. (2004). Dissociation of spatial attention and saccade preparation. PNAS, 101(43), 15541–15544.PubMedCrossRefGoogle Scholar
  81. Kato, M., & Miyauchi, S. (2003). Human precentral cortical activation patterns during saccade tasks: an fMRI comparison with activation during intentional eyeblink tasks. Neuroimage, 19, 1260–1272.PubMedCrossRefGoogle Scholar
  82. Kemmotsu, N., Villalobos, M. E., Gaffrey, M. S., Courchesne, E., & Müller, R.-A. (2005). Activity and functional connectivity of inferior frontal cortex associated with response conflict. Cognitive Brain Research, 24, 335–342.PubMedCrossRefGoogle Scholar
  83. Kemner, C., van der Geest, J., Verbaten, M., & van Engeland, H. (2004). In search of neurophysiological markers of pervasive developmental disorders: smooth pursuit eye movements? Journal of Neural Transmission, 111(12), 1617–1626.PubMedCrossRefGoogle Scholar
  84. Kemner, C., Verbaten, M. N., Cuperus, J. M., Camfferman, G., & van Engeland, H. (1998). Abnormal saccadic eye movements in autistic children. Journal of Autism and Developmental Disorders, 28, 61–67.PubMedCrossRefGoogle Scholar
  85. Kemper, T. L., & Bauman, M. L. (1993). The contribution of neuropathologic studies to the understanding of autism. Neurologic Clinics, 11(1), 175–187.PubMedGoogle Scholar
  86. Kleinhans, N., Akshoomoff, N., & Delis, D. C. (2005). Executive Functions in Autism and Asperger’s Disorder: Flexibility, Fluency, and Inhibition. Developmental Neuropsychology, 27(3), 379–401.PubMedCrossRefGoogle Scholar
  87. Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59(9), 809–816.PubMedCrossRefGoogle Scholar
  88. Knox, P. (2004a, June 07, 2004). Methods of measuring eye movement. Retrieved July 20, 2004, from∼pcknox/teaching/Eymovs/emeth.htm Google Scholar
  89. Knox, P. (2004b, June 07, 2004). The parameters of eye movement. Retrieved July 21, 2004, from∼pcknox/teaching/Eymovs/params.htm Google Scholar
  90. Koch, C., & Ullman, S. (1985). Shifts in visual attention: Towards the underlying circuitry. Human Neurobiology, 4, 219–222.PubMedGoogle Scholar
  91. Kolb, B., & Gibb, R. (2001). Early brain injury, plasticity, behavior. In C. A. Nelson & M. Luciana (Eds.), Handbook of developmental cognitive neuroscience (pp. 175–190). Cambridge (MA): MIT Press.Google Scholar
  92. Konen, C., Kleiser, R., Wittsack, H.-J., Bremmer, F., & Seitz, R. (2004). The encoding of saccadic eye movements within human posterior parietal cortex. Neuroimage, 22, 304–314.PubMedCrossRefGoogle Scholar
  93. Konishi, S., Nakajima, K., Uchida, I., Kameyama, M., Nakahara, K., Sekihara, K., et al. (1998). Transient activation of inferior prefrontal cortex during cognitive set shifting. Nat Neurosci, 1(1), 80–84.PubMedCrossRefGoogle Scholar
  94. Kowler, E., & Blaser, E. (1995). The accuracy and precision of saccades to small and large targets. Vision Research, 19, 619–632.CrossRefGoogle Scholar
  95. Koyama, M., Hasegawa, I., Osado, T., Adachi, Y., Nakahara, K., & Miyashita, Y. (2004). Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans. Neuron, 41, 795–807.PubMedCrossRefGoogle Scholar
  96. Krams, M., Rushworth, M. F., Deiber, M. P., Frackowiak, R. S., & Passingham, R. E. (1998). The preparation, execution and suppression of copied movements in the human brain. Experimental Brain Research, 120(3), 386–398.CrossRefGoogle Scholar
  97. Krauzlis, R. (2004). Recasting the smooth pursuit eye movement system. Journal of Neurophysiology, 91, 591–603.PubMedCrossRefGoogle Scholar
  98. Lee, M., Martin-Ruiz, C., Graham, A., Court, J., Jaros, E., Perry, R., et al. (2002). Nicotinic receptor abnormalities in the cerebellar cortex in autism. Brain, 125(Pt 7), 1483–1495.PubMedCrossRefGoogle Scholar
  99. Lengyel, D., Weinacht, S., Charlier, J., & Gottlob, I. (1998). The development of visual pursuit during the first months of life. Graefes Archive for Clinical and Experimental Ophthalmology, 236(6), 440–444.CrossRefGoogle Scholar
  100. Luna, B., Minshew, N. J., Garver, K. E., Lazar, N. A., Thulborn, K. R., Eddy, W. F., et al. (2002). Neocortical system abnormalities in autism: An fMRI study of spatial working memory. Neurology, 59(6), 834–840.PubMedGoogle Scholar
  101. Luna, B., Thulborn, K., Strojwas, M., McCurtain, B., Berman, R., Genovese, C., et al. (1998). Dorsal cortical regions subserving visually guided saccades in humans: An fMRI study. Cerebral Cortex, 8, 40–47.PubMedCrossRefGoogle Scholar
  102. Makino, Y., Yokosawa, K., Takeda, Y., & Kumada, T. (2004). Visual search and memory search engage extensive overlapping cerebral cortices: An fMRI study. Neuroimage, 23, 525–533.PubMedCrossRefGoogle Scholar
  103. Manjaly, Z., Bruning, N., Konrad, K., Marshall, J., Zilles, K., & Fink, G., et al. (2004). The neural mechanisms underlying local visual search in autistic adolescents. Paper presented at the OHBM, Budapest.Google Scholar
  104. Manjaly, Z., Marshall, J., Stephan, K., Gurd, J. M., Zilles, K., & Fink, G. (2003). In search of the hidden: an fMRI study with implications for the study of patients with autism and with acquired brain injury. Neuroimage, 19, 674–683.PubMedCrossRefGoogle Scholar
  105. Markus, J., Mundy, P., Morales, M., Delgado, C. E., & Yale, M. (2000). Individual differences in infant skills as predictors of child-caregiver joint attention and language. Social Development, 9(3), 302–315.CrossRefGoogle Scholar
  106. McPeek, R., & Keller, E. (2002). Saccade target selection in the superior colliculus during a visual search task. Journal of Neurophysiology, 88, 2019–2034.PubMedGoogle Scholar
  107. McPeek, R., & Keller, E. (2004). Deficits in saccade target selection after inactivation of superior colliculus. Nature Neuroscience, 7(7), 757–763.PubMedCrossRefGoogle Scholar
  108. Miller, L. M., & D’Esposito, M. (2005). Perceptual fusion and stimulus coincidence in the cross-modal integration of speech. J Neurosci, 25(25), 5884–5893.PubMedCrossRefGoogle Scholar
  109. Miller, M. T., Stromland, K., Ventura, L., Johansson, M., Bandim, J. M., & Gillberg, C. (2005). Autism associated with conditions characterized by developmental errors in early embryogenesis: a mini review. Int J Dev Neurosci, 23(2–3), 201–219.PubMedCrossRefGoogle Scholar
  110. Minshew, N. J., Luna, B., & Sweeney, J. A. (1999). Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology, 52(5), 917–922.PubMedGoogle Scholar
  111. Minshew, N. J., Sweeney, J., & Luna, B. (2002). Autism as a selective disorder of complex information processing and underdevelopment of neocortical systems. Molecular Psychiatry, 7(Suppl 2), S14–15.PubMedCrossRefGoogle Scholar
  112. Mort, D., Perry, R., Mannan, S., Hodgson, T., Anderson, E., Quest, R., et al. (2003). Differential cortical activation during voluntary and reflexive saccades in man. Neuroimage, 18, 231–246.PubMedCrossRefGoogle Scholar
  113. Mottron, L., Burack, J., Iarocci, G., Belleville, S., & Enns, J. (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.Google Scholar
  114. Muggleton, N., Juan, C., Cowey, A., & Walsh, V. (2003). Human frontal eye fields and visual search. Journal of Neurophysiology, 89, 3340–3343.PubMedCrossRefGoogle Scholar
  115. Mundy, P., Sigman, M., Ungerer, J., & Sherman, T. (1986). Defining the social deficits of autism: the contribution of non-verbal communication measures. Journal of Child Psychology and Psychiatry and Allied Disciplines, 27(5), 657–669.Google Scholar
  116. Munoz, D. P., Broughton, J. R., Goldring, J. E., & Armstrong, I. T. (1998). Age-related performance of human subjects on saccadic eye movement tasks. Experimental Brain Research, 121(4), 391–400.CrossRefGoogle Scholar
  117. Murphy, A., Thompson, K., & Schall, J. (2001). Dynamic dissociation of visual selection from saccade programming in frontal eye field. Journal of Neurophysiology, 86, 2634–2637.Google Scholar
  118. Müller, N., Donner, T., Bartelt, O., Brandt, S., Villringer, A., & Kleinschmidt, A. (2003). The functional neuroanatomy of visual conjunction search: A parametric fMRI study. Neuroimage, 20, 1578–1590.PubMedCrossRefGoogle Scholar
  119. Müller, R.-A. (2005). Neurocognitive studies of language impairment: The ‘bottom-up’ approach. Applied Psycholinguistics, 26, 65–78.CrossRefGoogle Scholar
  120. Müller, R.-A., & Basho, S. (2004). Are nonlinguistic functions in “Broca’s area” prerequisites for language acquisition? FMRI findings from an ontogenetic viewpoint. Brain and Language, 89, 329–336.PubMedCrossRefGoogle Scholar
  121. Müller, R.-A., & Courchesne, E. (2000). The duplicity of plasticity: a conceptual approach to the study of early lesion and developmental disorders. In M. Ernst & J. Rumsey (Eds.), The foundation and future of functional neuroimaging in child psychiatry (pp. 335–365). New York: Cambridge UP.Google Scholar
  122. Natsopoulos, D., Kiosseoglou, G., Xeromeritou, A., & Alevriadou, A. (1998). Do the hands talk on mind’s behalf? Differences in language ability between left- and right-handed children. Brain and Language, 64(2), 182–214.PubMedCrossRefGoogle Scholar
  123. Nitschke, M., Binkofski, F., Buccino, G., Posse, S., Erdmann, C., Kompf, D., et al. (2004). Activation of cerebellar hemispheres in spatial memorization of saccadic eye movements: An fMRI study. Human Brain Mapping, 22, 155–164.PubMedCrossRefGoogle Scholar
  124. Nobre, A., Coull, J., Walsh, V., & Frith, C. (2003). Brain activations during visual search: contributions of search efficiency versus feature binding. NeuroImage, 18, 91–103.PubMedCrossRefGoogle Scholar
  125. Nobre, A., Gitelman, D., Dias, E., & Mesulam, M. (2000). Covert visual spatial orienting and saccades: Overlapping neural systems. Neuroimage, 11, 210–216.PubMedCrossRefGoogle Scholar
  126. Nobre, A., Sebestyen, G., Gitelman, D., Frith, C., & Mesulam, M. (2002). Filtering of distractors during visual search studied by positron emission tomography. Neuroimage, 16, 968–976.PubMedCrossRefGoogle Scholar
  127. Nowinski, C. V., Minshew, N. J., Luna, B., Takarae, Y., & Sweeney, J. A. (2005). Oculomotor studies of cerebellar function in autism. Psychiatry Res, 137(1–2), 11–19.PubMedCrossRefGoogle Scholar
  128. O’Riordan, M., Plaisted, K., Driver, J., & Baron-Cohen, S. (2001). Superior visual search in autism. Journal of Experimental Psychology: Human Perception and Performance, 27(3), 719–730.PubMedCrossRefGoogle Scholar
  129. O’Riordan, M. A. (2004). Superior visual search in adults with autism. Autism, 8(3), 229–248.PubMedCrossRefGoogle Scholar
  130. Palmen, S. J., & van Engeland, H. (2004). Review on structural neuroimaging findings in autism. Journal of Neural Transmission, 111(7), 903–929.PubMedCrossRefGoogle Scholar
  131. Pelphrey, K. A., Sasson, N. J., Reznick, J. S., Paul, G., Goldman, B. D., & Piven, J. (2002). Visual scanning of faces in autism. J Autism Dev Disord, 32(4), 249–261.PubMedCrossRefGoogle Scholar
  132. Pierce, K., Haist, F., Sedaghat, F., & Courchesne, E. (2004). The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain, 127(Pt 12), 2703–2716.PubMedCrossRefGoogle Scholar
  133. Pierce, K., Müller, R.-A., Ambrose, J. B., Allen, G., & Courchesne, E. (2001). Face processing occurs outside the ‘fusiform face area’ in autism: evidence from functional MRI. Brain, 124, 2059–2073.PubMedCrossRefGoogle Scholar
  134. Pierrot-Deseilligny, C., Muri, R., & Ploner, C. (2003). Decisional role of the dorsolateral prefrontal cortex in ocular motor behavior. Brain, 126, 1460–1473.PubMedCrossRefGoogle Scholar
  135. Plaisted, K., O’Riordan, M., & Baron-Cohen, S. (1998). Enhanced visual search for a conjunctive target in autism: a research note. Journal of Child Psychology and Psychiatry and Allied Disciplines, 39(5), 777–783.Google Scholar
  136. Quinlan, P., & Humphreys, G. (1987). Visual search for targets defined by color, shape, and size: An examination of the task constraints on feature and conjunction searches. Perception and Psychophysics, 41, 455–472.PubMedGoogle Scholar
  137. Richards, J. E. (1989). Development and stability in visual sustained attention in 14, 20, and 26 week old infants. Psychophysiology, 26(4), 422–430.PubMedCrossRefGoogle Scholar
  138. Richards, J. E. (2001). Attention in young infants: a dvelopmental psychophysiological perspective. In C. A. Nelson & M. Luciana (Eds.), Handbook of developmental cognitive neuroscience (pp. 321–338). Cambridge, Mass: MIT Press.Google Scholar
  139. Richards, J. E., & Holley, F. B. (1999). Infant attention and the development of smooth pursuit tracking. Developmental Psychology, 35(3), 856–867.PubMedCrossRefGoogle Scholar
  140. Ring, H., Baron-Cohen, S., Wheelwright, S., Williams, S., Brammer, M., Andrew, C., et al. (1999). Cerebral correlates of preserved cognitive skills in autism. Brain, 122, 1305–1315.PubMedCrossRefGoogle Scholar
  141. 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(7), 862–866.PubMedGoogle Scholar
  142. Robinson, F., & Fuchs, A. (2001). The role of the cerebellum in voluntary eye movements. Annual Review of Neuroscience, 24, 981–1004.PubMedCrossRefGoogle Scholar
  143. Rodier, P. M. (2002). Converging evidence for brain stem injury in autism. Dev Psychopathol, 14(3), 537–557.PubMedCrossRefGoogle Scholar
  144. Rodier, P. M., Ingram, J. L., Tisdale, B., Nelson, S., & Romano, J. (1996). Embryological origin for autism: developmental anomalies of the cranial nerve motor nuclei. Journal of Comparative Neurology, 370(2), 247–261.PubMedCrossRefGoogle Scholar
  145. Rogers, S. J., Bennetto, L., McEvoy, R., & Pennington, B. F. (1996). Imitation and pantomime in high-functioning adolescents with autism spectrum disorders. Child Development, 67(5), 2060–2073.PubMedCrossRefGoogle Scholar
  146. 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 and Allied Disciplines, 44(5), 763–781.Google Scholar
  147. Rosano, C., Krisky, C., Welling, J., Eddy, W., Luna, B., Thulborn, K., et al. (2002). Pursuit and saccadic eye movement subregions in human frontal eye field: a high-resolution fMRI investigation. Cerebral Cortex, 12, 107–115.PubMedCrossRefGoogle Scholar
  148. Rosenhall, U., Johansson, E., & Gillberg, C. (1988). Oculomotor findings in autistic children. J Laryngology and Otology, 102, 435–439.Google Scholar
  149. Rubia, K., Russell, T., Overmeyer, S., Brammer, M. J., Bullmore, E. T., Sharma, T., et al. (2001). Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage, 13(2), 250–261.PubMedCrossRefGoogle Scholar
  150. Ruff, H., & Lawson, K. (1990). Development of sustained, focused attention in young children during free play. Developmental Psychology, 26(1), 85–93.CrossRefGoogle Scholar
  151. Sadato, N., Okada, T., Honda, M., & Yonekura, Y. (2002). Critical period for cross-modal plasticity in blind humans: a functional MRI study. Neuroimage, 16(2), 389–400.PubMedCrossRefGoogle Scholar
  152. Schall, J., & Hanes, D. (1998). Neural mechanisms of selection and control of visually guided movements. Neural Networks, 11, 1241–1251.PubMedCrossRefGoogle Scholar
  153. Schlagg-Rey, M., Schlag, J., & Dassonville, P. (1992). How the frontal eye field can impose a saccade goal on superior colliculus neurons. Journal of Neurophysiology, 67(4), 1003–1005.Google Scholar
  154. Schultz, R. T., Gauthier, I., Klin, A., Fulbright, R. K., Anderson, A. W., Volkmar, F., et al. (2000). Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome [see comments]. Archives of General Psychiatry, 57(4), 331–340.PubMedCrossRefGoogle Scholar
  155. Schumann, C. M., Hamstra, J., Goodlin-Jones, B. L., Lotspeich, L. J., Kwon, H., Buonocore, M. H., et al. (2004). The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J Neurosci, 24(28), 6392–6401.PubMedCrossRefGoogle Scholar
  156. Shah, A., & Frith, U. (1983). An islet of ability in autistic children: a research note. Journal of Child Psychology and Psychiatry and Allied Disciplines, 24, 613–620.Google Scholar
  157. Shulman, G., McAvoy, M., Cowan, M., Astafiev, S., d’Avossa, G., & Corbetta, M. (2003). Quantitative analysis of attention and detection signals during visual search. Journal of Neurophysiology, 90(5), 3384–3397.PubMedCrossRefGoogle Scholar
  158. Sigman, M. D., Kasari, C., Kwon, J. H., & Yirmiya, N. (1992). Responses to the negative emotions of others by autistic, mentally retarded, and normal children. Child Development, 63(4), 796–807.PubMedCrossRefGoogle Scholar
  159. Sparks, B. F., Friedman, S. D., Shaw, D. W., Aylward, E. H., Echelard, D., Artru, A. A., et al. (2002). Brain structural abnormalities in young children with autism spectrum disorder. Neurology, 59(2), 184–192.PubMedGoogle Scholar
  160. Stanton, G., Bruce, C., & Goldberg, M. (1995). Topography of projections to posterior cortical areas from the macaque frontal eye fields. Journal of Comparative Neurology, 353, 291–305.PubMedCrossRefGoogle Scholar
  161. Sur, M., & Leamey, C. A. (2001). Development and plasticity of cortical areas and networks. Nat Rev Neurosci, 2(4), 251–262.PubMedCrossRefGoogle Scholar
  162. Sweeney, J., Takarae, Y., Macmillan, C., Luna, B., & Minshew, N. (2004). Eye movements in neurodevelopmental disorders. Current Opinion in Neurology, 17, 37–42.PubMedCrossRefGoogle Scholar
  163. Sweeten, T. L., Posey, D. J., Shekhar, A., & McDougle, C. J. (2002). The amygdala and related structures in the pathophysiology of autism. Pharmacol Biochem Behav, 71(3), 449–455.PubMedCrossRefGoogle Scholar
  164. Takagi, M., Zee, D., & Tamargo, R. (1998). Effects of lesions of the oculomotor vermis on eye movements in primate: Saccades. Journal of Neurophysiology, 80(4), 1911–1931.PubMedGoogle Scholar
  165. Takarae, Y., Minshew, N., Luna, B., Krisky, C., & Sweeney, J. (2004). Pursuit eye movement deficits in autism. Brain, 127, 2584–2594.PubMedCrossRefGoogle Scholar
  166. Thomas, M., & Karmiloff-Smith, A. (2002). Are developmental disorders like cases of adult brain damage? Implications from connectionist modeling. Behavioral and Brain Sciences, 25(6), 727–750.PubMedCrossRefGoogle Scholar
  167. Thompson-Schill, S. L., D’Esposito, M., Aguirre, G. K., & Farah, M. J. (1997). Role of left inferior prefrontal cortex in retrieval of semantic knowledge: A reevaluation. Proceedings of the National Academy of Sciences of the United States of America, 94(26), 14792–14797.PubMedCrossRefGoogle Scholar
  168. Tomasello, M., & Kruger, A. C. (1992). Joint attention on actions: acquiring verbs in ostensive and non-ostensive contexts. Journal of Child Language, 19(2), 311–333.PubMedCrossRefGoogle Scholar
  169. Townsend, J., & Courchesne, E. (1994). Parietal damage and narrow “spotlight” spatial attention. Journal of Cognitive Neuroscience, 6, 220–232.CrossRefGoogle Scholar
  170. Townsend, J., Courchesne, E., & Egaas, B. (1996). Slowed orienting of covert visual-spatial attention in autism: Specific deficits associated with cerebellar and parietal abnormality. Development and Psychopathology, 8, 563–584.CrossRefGoogle Scholar
  171. Treisman, A., & Gelade, G. (1980). A feature integration theory of attention. Cognitive Psychology, 12, 97–136.PubMedCrossRefGoogle Scholar
  172. van der Geest, J., Kemner, C., Camfferman, G., Verbaten, M., & van Engeland, H. (2001). Eye movements, visual attention, and autism: a saccadic reaction time study using the gap and overlap paradigm. Biological Psychiatry, 50, 614–619.PubMedCrossRefGoogle Scholar
  173. Verghese, P. (2001). Visual search and attention: a signal detection theory approach. Neuron, 31, 523–545.PubMedCrossRefGoogle Scholar
  174. Wainwright-Sharpe, J., & Bryson, S. (1993). Visual orienting deficits in high-functioning people with autism. Journal of Autism and Developmental Disorders, 23, 1–13.CrossRefGoogle Scholar
  175. Wainwright-Sharpe, J., & Bryson, S. (1996). Visual-spatial orienting in autism. Journal of Autism and Developmental Disorders, 26, 423–438.CrossRefGoogle Scholar
  176. Wilkinson, D., Halligan, P., Henson, R., & Dolan, R. (2002). The effects of interdistracter similarity on search processes in superior parietal cortex. Neuroimage, 15, 611–619.PubMedCrossRefGoogle Scholar
  177. Williams, J. H., Whiten, A., & Singh, T. (2004). A systematic review of action imitation in autistic spectrum disorders. Journal of Autism & Developmental Disorders, 34(3), 285–299.CrossRefGoogle Scholar
  178. Witkin, H., Oltman, P., Raskin, E., & Karp, S. (1971). Group embedded figures test manual. Palo Alto: Consulting Psychologists Press.Google Scholar
  179. Wolfe, J., Cave, K., & Franzel, S. (1989). Guided search: an alternative to the feature integration model for visual search. Journal of Experimental Psychology: Human Perception and Performance, 15, 419–433.PubMedCrossRefGoogle Scholar
  180. Wolfe, J., & Horowitz, T. (2004). What attributes guide the deployment of visual attention and how do they do it? Nature, 5, 1–7.Google Scholar
  181. Zilbovicius, M., Boddaert, N., Belin, P., Poline, J. B., Remy, P., Mangin, J. F., et al. (2000). Temporal lobe dysfunction in childhood autism: a PET study. Positron emission tomography. American Journal of Psychiatry, 157(12), 1988–1993.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2006

Authors and Affiliations

  • Laurie A. Brenner
    • 1
  • Katherine C. Turner
    • 1
  • Ralph-Axel Müller
    • 1
    • 2
  1. 1.Brain Development Imaging Laboratory, Department of PsychologySan Diego State UniversitySan DiegoUSA
  2. 2.Department of Cognitive ScienceUniversity of CaliforniaSan DiegoUSA

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