Skip to main content
Log in

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

  • Original Paper
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Akshoomoff, N., Courchesne, E., & Townsend, J. (1997). Attention coordination and anticipatory control. International Review of Neurobiology, 41, 575–598.

    PubMed  Google Scholar 

  • Akshoomoff, N., Pierce, K., & Courchesne, E. (2002). The neurobiological basis of autism from a developmental perspective. Development and Psychopathology, 14(3), 613–634.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Baltaxe, C. A., & Simmons, J. Q. (1975). Language in childhood psychosis: a review. Journal of Speech and Hearing Disorders, 40(4), 439–458.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Brooks, R., & Meltzoff, A. N. (2005). The development of gaze following and its relation to language. Developmental Science, 8(6), 535–543.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Buccino, G., Binkofski, F., & Riggio, L. (2004). The mirror neuron system and action recognition. Brain and Language, 89(2), 370–376.

    Article  PubMed  Google Scholar 

  • Burack, J. (1994). Selective attention deficits in persons with autism: preliminary evidence of an inefficient attentional lens. Journal of Abnormal Psychology, 103, 535–543.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • Carper, R. A., & Courchesne, E. (2005). Localized enlargement of the frontal cortex in early autism. Biological Psychiatry, 57(2), 126–133.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Colombo, J. (2001). The development of visual attention in infancy. Annual Review of Psychology, 52, 337–367.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Damasio, A. R., & Maurer, R. G. (1978). A neurological model for childhood autism. Archives of Neurology, 35, 777–786.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Delis, D., Kaplan, E., & Kramer, J. (2001). Delis-Kaplan executive function system. San Antonio, TX: The Psychological Corporation.

    Google Scholar 

  • Desimone, R., & Duncan, J. (1995). Neural mechanisms of selective visual attention. Annual Review of Neuroscience, 18, 193–222.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Deubel, H., & Schneider, W. (1996). Saccade target selection and object recognition: evidence for a common attentional mechanism. Vision Research, 36, 1827–1837.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Duncan, J., & Humphreys, G. (1989). Visual search and stimulus similarity. Psychological Review, 96, 433–458.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Findlay, J., & Gilchrist, I. (2003). Active vision: The physiology of looking and seeing. New York: Oxford University Press.

    Google Scholar 

  • Frith, U. (1989). Autism: Explaining the enigma. Oxford: Blackwell.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Gaymard, B., Ploner, C., Rivaud, S., Vermersch, A., & Pierrot-Deseilligny, C. (1998). Cortical control of saccades. Experimental Brain Research, 123, 159–163.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Hanes, D., & Wurtz, R. (2001). Interaction of the frontal eye field and superior colliculus for saccade generation. Journal of Neurophysiology, 85, 804–815.

    PubMed  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • Hunt, R., & Ellis, H. (1999). Fundamentals of cognitive psychology (6th ed.). Boston: McGraw-Hill College.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Johnson, M. H. (1995). The inhibition of automatic saccades in early infancy. Developmental Psychobiology, 28(5), 281–291.

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • Juan, C., Shorter-Jacobi, S., & Schall, J. (2004). Dissociation of spatial attention and saccade preparation. PNAS, 101(43), 15541–15544.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Kemper, T. L., & Bauman, M. L. (1993). The contribution of neuropathologic studies to the understanding of autism. Neurologic Clinics, 11(1), 175–187.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Knox, P. (2004a, June 07, 2004). Methods of measuring eye movement. Retrieved July 20, 2004, from www.liv.ac.uk/∼pcknox/teaching/Eymovs/emeth.htm

  • Knox, P. (2004b, June 07, 2004). The parameters of eye movement. Retrieved July 21, 2004, from www.liv.ac.uk/∼pcknox/teaching/Eymovs/params.htm

  • Koch, C., & Ullman, S. (1985). Shifts in visual attention: Towards the underlying circuitry. Human Neurobiology, 4, 219–222.

    PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Kowler, E., & Blaser, E. (1995). The accuracy and precision of saccades to small and large targets. Vision Research, 19, 619–632.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Krauzlis, R. (2004). Recasting the smooth pursuit eye movement system. Journal of Neurophysiology, 91, 591–603.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • McPeek, R., & Keller, E. (2002). Saccade target selection in the superior colliculus during a visual search task. Journal of Neurophysiology, 88, 2019–2034.

    PubMed  Google Scholar 

  • McPeek, R., & Keller, E. (2004). Deficits in saccade target selection after inactivation of superior colliculus. Nature Neuroscience, 7(7), 757–763.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Muggleton, N., Juan, C., Cowey, A., & Walsh, V. (2003). Human frontal eye fields and visual search. Journal of Neurophysiology, 89, 3340–3343.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • Müller, R.-A. (2005). Neurocognitive studies of language impairment: The ‘bottom-up’ approach. Applied Psycholinguistics, 26, 65–78.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Nobre, A., Gitelman, D., Dias, E., & Mesulam, M. (2000). Covert visual spatial orienting and saccades: Overlapping neural systems. Neuroimage, 11, 210–216.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • O’Riordan, M. A. (2004). Superior visual search in adults with autism. Autism, 8(3), 229–248.

    Article  PubMed  Google Scholar 

  • Palmen, S. J., & van Engeland, H. (2004). Review on structural neuroimaging findings in autism. Journal of Neural Transmission, 111(7), 903–929.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Pierrot-Deseilligny, C., Muri, R., & Ploner, C. (2003). Decisional role of the dorsolateral prefrontal cortex in ocular motor behavior. Brain, 126, 1460–1473.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • Richards, J. E. (1989). Development and stability in visual sustained attention in 14, 20, and 26 week old infants. Psychophysiology, 26(4), 422–430.

    Article  PubMed  Google Scholar 

  • 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 

  • Richards, J. E., & Holley, F. B. (1999). Infant attention and the development of smooth pursuit tracking. Developmental Psychology, 35(3), 856–867.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  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(7), 862–866.

    PubMed  Google Scholar 

  • Robinson, F., & Fuchs, A. (2001). The role of the cerebellum in voluntary eye movements. Annual Review of Neuroscience, 24, 981–1004.

    Article  PubMed  Google Scholar 

  • Rodier, P. M. (2002). Converging evidence for brain stem injury in autism. Dev Psychopathol, 14(3), 537–557.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  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 and Allied Disciplines, 44(5), 763–781.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Rosenhall, U., Johansson, E., & Gillberg, C. (1988). Oculomotor findings in autistic children. J Laryngology and Otology, 102, 435–439.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Ruff, H., & Lawson, K. (1990). Development of sustained, focused attention in young children during free play. Developmental Psychology, 26(1), 85–93.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Schall, J., & Hanes, D. (1998). Neural mechanisms of selection and control of visually guided movements. Neural Networks, 11, 1241–1251.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Sur, M., & Leamey, C. A. (2001). Development and plasticity of cortical areas and networks. Nat Rev Neurosci, 2(4), 251–262.

    Article  PubMed  Google Scholar 

  • Sweeney, J., Takarae, Y., Macmillan, C., Luna, B., & Minshew, N. (2004). Eye movements in neurodevelopmental disorders. Current Opinion in Neurology, 17, 37–42.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Takarae, Y., Minshew, N., Luna, B., Krisky, C., & Sweeney, J. (2004). Pursuit eye movement deficits in autism. Brain, 127, 2584–2594.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Townsend, J., & Courchesne, E. (1994). Parietal damage and narrow “spotlight” spatial attention. Journal of Cognitive Neuroscience, 6, 220–232.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Treisman, A., & Gelade, G. (1980). A feature integration theory of attention. Cognitive Psychology, 12, 97–136.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Verghese, P. (2001). Visual search and attention: a signal detection theory approach. Neuron, 31, 523–545.

    Article  PubMed  Google Scholar 

  • Wainwright-Sharpe, J., & Bryson, S. (1993). Visual orienting deficits in high-functioning people with autism. Journal of Autism and Developmental Disorders, 23, 1–13.

    Article  Google Scholar 

  • Wainwright-Sharpe, J., & Bryson, S. (1996). Visual-spatial orienting in autism. Journal of Autism and Developmental Disorders, 26, 423–438.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Witkin, H., Oltman, P., Raskin, E., & Karp, S. (1971). Group embedded figures test manual. Palo Alto: Consulting Psychologists Press.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

Download references

Acknowledgement

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

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ralph-Axel Müller.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brenner, L.A., Turner, K.C. & Müller, RA. Eye Movement and Visual Search: Are There Elementary Abnormalities in Autism?. J Autism Dev Disord 37, 1289–1309 (2007). https://doi.org/10.1007/s10803-006-0277-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-006-0277-9

Keywords

Navigation