DOI: 10.3724/SP.J.1042.2020.00098

Advances in Psychological Science (心理科学进展) 2020/28:1 PP.98-110

The characteristics and neural mechanisms of visual orienting and visual search in autism spectrum disorders

Orienting network is an important part of attention system and it includes two major tasks:visual orienting and visual search. For these two tasks, typically developed group shows similar neural mechanisms. However, from a perspective of attention to non-social information, different behavioral patterns were observed between visual orienting and visual search in autism spectrum disorder (ASD) group. Regarding visual orienting, the consensus is that ASD individuals are intact in attentional shift but have difficulty in attentional disengagement; however, this conclusion is still controversial. Regarding visual search, ASD individuals have superior search ability, but its time sequence and reasons deserves further exploration. Future studies should identify the hemispherical symmetry of ASD individuals in visual orienting task, the underlying mechanisms of visual search advantage, and the relationships between visual orienting and visual search in ASD populations.

Key words:autism,non-social information,visual orienting,visual search,neural mechanisms

ReleaseDate:2019-12-28 14:18:56

卜凡帅, 赵微, 荆伟. (2016). 学前自闭症谱系障碍儿童视觉搜索优势:来自眼动和瞳孔测量的联合证据. 中国特殊教育, (6), 52-58.

纪皓月, 王莉, 蒋毅. (2018). 孤独症谱系障碍患者社会性注意行为的异常表现及其神经机制. 科学通报, 63(15), 1428-1437.

孙岩, 房林, 王亭予, 崔丽. (2018). 自闭症谱系障碍者抑制控制的影响因素及神经机制. 心理科学进展, 26(8), 1450-1464.

魏萍, 周晓林. (2011). 任务维度和任务无关维度干扰信息的同质性影响视觉搜索的神经机制. 心理科学进展, 19(6), 794-802.

American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders:DSM 5. New York:American Psychiatric Publishing.

Baldassi, S., Pei, F., Megna, N., Recupero, G., Viespoli, M., Igliozzi, R.,… Cioni, G. (2009). Search superiority in autism within, but not outside the crowding regime. Vision Research, 49(16), 2151-2156.

Barras, C., & Kerzel, D. (2017). Salient-but-irrelevant stimuli cause attentional capture in difficult, but attentional suppression in easy visual search. Psychophysiology, 54(12), 1826-1838.

Bayliss, A. P., & Kritikos, A. (2010). Brief report:Perceptual load and the autism spectrum in typically developed individuals. Journal of Autism and Developmental Disorders, 41(11), 1573-1578.

Bedford, R., Pickles, A., Gliga, T., Elsabbagh, M., Charman, T., Johnson, M. H., & Team, B. (2014). Additive effects of social and non-social attention during infancy relate to later autism spectrum disorder. Developmental Science, 17(4), 612-620.

Bishop, H. J., Biasini, F. J., & Stavrinos, D. (2017). Social and non-social hazard response in drivers with autism spectrum disorder. Journal of Autism and Developmental Disorders, 47(4), 905-917.

Blaser, E., Eglington, L., Carter, A. S., & Kaldy, Z. (2014). Pupillometry reveals a mechanism for the autism spectrum disorder (ASD) advantage in visual tasks. Scientific Reports, 4, 4301.

Booth, R. D. L., & Happé, F. G. E. (2016). Evidence of reduced global processing in autism spectrum disorder. Journal of Autism and Developmental Disorders, 48(4), 1397-1408.

Braukmann, R., Lloyd-Fox, S., Blasi, A., Johnson, M. H., Bekkering, H., Buitelaar, J. K., & Hunnius, S. (2018). Diminished socially selective neural processing in 5-month-old infants at high familial risk of autism. European Journal of Neuroscience, 47(6), 720-728.

Bryson, S., Garon, N., McMullen, T., Brian, J., Zwaigenbaum, L., Armstrong, V.,… Szatmari, P. (2017). Impaired disengagement of attention and its relationship to emotional distress in infants at high-risk for autism spectrum disorder. Journal of Clinical and Experimental Neuropsychology, 40(5), 487-501.

Caron, M.-J., Mottron, L., Rainville, C., & Chouinard, S. (2004). Do high functioning persons with autism present superior spatial abilities? Neuropsychologia, 42(4), 467-481.

Cheung, C. H. M., Bedford, R., Johnson, M. H., Charman, T., Gliga, T., & Team, B. (2016). Visual search performance in infants associates with later ASD diagnosis. Developmental Cognitive Neuroscience, 29, 4-10.

Constable, P. A., Solomon, J. A., Gaigg, S. B., & Bowler, D. M. (2010). Crowding and visual search in high functioning adults with autism spectrum disorder. Clinical Optometry, 2, 93-103.

Coull, J. T., Walsh, V., Frith, C. D., & Nobre, A. C. (2003). Distinct neural substrates for visual search amongst spatial versus temporal distractors. Cognitive Brain Research, 17(2), 368-379.

Courchesne, E., Press, G. A., & Yeung-Courchesne, R. (1993). Parietal lobe abnormalities detected with MR in patients with infantile autism. American Journal of Roentgenology, 160(2), 387-393.

Csibra, G., Johnson, M. H., & Tucker, L. A. (1997). Attention and oculomotor control:A high-density ERP study of the gap effect. Neuropsychologia, 35(6), 855-865.

Dakin, S., & Frith, U. (2005). Vagaries of visual perception in autism. Neuron, 48(3), 497-507.

Donner, T., Kettermann, A., Diesch, E., Ostendorf, F., Villringer, A., & Brandt, S. A. (2000). Involvement of the human frontal eye field and multiple parietal areas in covert visual selection during conjunction search. European Journal of Neuroscience, 12(9), 3407-3414.

Donner, T. H., Kettermann, A., Diesch, E., Ostendorf, F., Villringer, A., & Brandt, S. A. (2002). Visual feature and conjunction searches of equal difficulty engage only partially overlapping frontoparietal networks. Neuroimage, 15(1), 16-25.

Elison, J. T., Sasson, N. J., Turner-Brown, L. M., Dichter, G. S., & Bodfish, J. W. (2012). Age trends in visual exploration of social and nonsocial information in children with autism. Research in Autism Spectrum Disorders, 6(2), 842-851.

Elsabbagh, M., Fernandes, J., Webb, S. J., Dawson, G., Charman, T., Johnson, M. H., & Team, B. A. S. O. I. S. (2013). Disengagement of visual attention in infancy is associated with emerging autism in toddlerhood. Biological Psychiatry, 74(3), 189-194.

Elsabbagh, M., Volein, A., Holmboe, K., Tucker, L., Csibra, G., Baron-Cohen, S.,… Johnson, M. H. (2009). Visual orienting in the early broader autism phenotype:Disengagement and facilitation. Journal of Child Psychology Psychiatry, 50(5), 637-642.

Fan, J., Bernardi, S., van Dam, N. T., Anagnostou, E., Gu, X. S., Martin, L.,… Hof, P. R. (2012). Functional deficits of the attentional networks in autism. Brain and Behavior, 2(5), 647-660.

Fischer, J., Koldewyn, K., Jiang, Y. V., & Kanwisher, N. (2014). Unimpaired attentional disengagement and social orienting in children with autism. Clinical Psychological Science, 2(2), 214-223.

Frith, U., & Happé, F. (1994). Autism:Beyond "theory of mind". Cognition, 50(1-3), 115-132.

Gammer, I., Bedford, R., Elsabbagh, M., Garwood, H., Pasco, G., Tucker, L.,… Team, B. (2015). Behavioural markers for autism in infancy:Scores on the autism observational scale for infants in a prospective study of at-risk siblings. Infant Behavior and Development, 38, 107-115.

Geschwind, D. H. (2009). Advances in autism. Annual Review of Medicine, 60, 367-380.

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.

Greene, D. J., Colich, N., Iacoboni, M., Zaidel, E., Bookheimer, S. Y., & Dapretto, M. (2011). Atypical neural networks for social orienting in autism spectrum disorders. Neuroimage, 56(1), 354-362.

Happé, F. G. E., & Booth, R. D. L. (2008). The power of the positive:Revisiting weak coherence in autism spectrum disorders. The Quarterly Journal of Experimental Psychology, 61(1), 50-63.

Hessels, R. S., Hooge, I. T. C., Snijders, T. M., & Kemner, C. (2014). Is there a limit to the superiority of individuals with ASD in visual search? Journal of Autism and Developmental Disorders, 44(2), 443-451.

Itti, L., & Koch, C. (2000). A saliency-based search mechanism for overt and covert shifts of visual attention. Vision Research, 40(10-12), 1489-1506.

Jobs, E. N., Falck-Ytter, T., & Bölte, S. (2018). Local and global visual processing in 3-year-olds with and without autism. Journal of Autism and Developmental Disorders, 48(6), 2249-2257.

Jones, E. J. H., Venema, K., Earl, R., Lowy, R., Barnes, K., Estes, A.,… Webb, S. J. (2016). Reduced engagement with social stimuli in 6-month-old infants with later autism spectrum disorder:A longitudinal prospective study of infants at high familial risk. Journal of Neurodevelopmental Disorders, 8, 1-20.

Joseph, R. M., Keehn, B., Connolly, C., Wolfe, J. M., & Horowitz, T. S. (2009). Why is visual search superior in autism spectrum disorder? Developmental Science, 12(6), 1083-1096.

Kaldy, Z., Giserman, I., Carter, A. S., & Blaser, E. (2016). The mechanisms underlying the ASD advantage in visual search. Journal of Autism and Developmental Disorders, 46(5), 1513-1527.

Kawakubo, Y., Kasai, K., Okazaki, S., Hosokawa-Kakurai, M., Watanabe, K.-I., Kuwabara, H.,… Maekawa, H. (2007). Electrophysiological abnormalities of spatial attention in adults with autism during the gap overlap task. Clinical Neurophysiology, 118(7), 1464-1471.

Keehn, B., Brenner, L., Palmer, E., Lincoln, A. J., & Müller, R.-A. (2008). Functional brain organization for visual search in ASD. Journal of the International Neuropsychological Society, 14(6), 990-1003.

Keehn, B., & Joseph, R. M. (2016). Slowed search in the context of unimpaired grouping in autism:Evidence from multiple conjunction search. Autism Research, 9(3), 333-339.

Keehn, B., Shih, P., Brenner, L. A., Townsend, J., & Müller, R.-A. (2013). Functional connectivity for an "island of sparing" in autism spectrum disorder:An fMRI study of visual search. Human Brain Mapping, 34(10), 2524-2537.

Kelly, D. J., Walker, R., & Norbury, C. F. (2012). Deficits in volitional oculomotor control align with language status in autism spectrum disorders. Developmental Science, 16(1), 56-66.

Landry, R., & Bryson, S. E. (2004). Impaired disengagement of attention in young children with autism. Journal of Child Psychology and Psychiatry, 45(6), 1115-1122.

Lavie, N. (1995). Perceptual load as a necessary condition for selective attention. Journal of Experimental Psychology:Human Perception and Performance, 21(3), 451-468.

Leekam, S. (2016). Social cognitive impairment and autism:What are we trying to explain? Philosophical Transactions of the Royal Society Biological Sciences, 371(1686), 1-8.

Lloyd-Fox, S., Richards, J. E., Blasi, A., Murphy, D. G. M., Elwell, C. E., & Johnson, M. H. (2014). Coregistering functional near-infrared spectroscopy with underlying cortical areas in infants. Neurophotonics, 1(2), 025006.

Luck, S. J., & Hillyard, S. A. (1994a). Spatial filtering during visual search:Evidence from human electrophysiology. Journal of Experimental Psychology:Human Perception and Performance, 20(5), 1000-1014.

Luck, S. J., & Hillyard, S. A. (1994b). Electrophysiological correlates of feature analysis during visual search. Psychophysiology, 31(3), 291-308.

Madipakkam, A. R., Rothkirch, M., Dziobek, I., & Sterzer, P. (2017). Unconscious avoidance of eye contact in autism spectrum disorder. Scientific Reports, 7(1), 13378.

Marshall, D. R. (2011). Impaired visual disengagement in autism:Can this be due to stimulus effects and inherent interest? (Unpublished doctorial dissertation), Durham University.

Nayar, K., Voyles, A. C., Kiorpes, L., & Martino, A. D. (2017). Global and local visual processing in autism:An objective assessment approach. Autism Research, 10(8), 1392-1404.

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

O'Riordan, M. A., Plaisted, K. C., Driver, J., & Baron-Cohen, S. (2001). Superior visual search in autism. Journal of Experimental Psychology:Human Perception and Performance, 27(3), 719-730.

Petersen, S. E., & Posner, M. I. (2012). The attention system of the human brain:20 years after. Annual Review of Neuroscience, 35, 73-89.

Pierrot-Deseilligny, C., Rivaud, S., Gaymard, B., Müri, R., & Vermersch, A.-I. (1995). Cortical control of saccades. Neurological Progress, 37(5), 557-567.

Pierrot-Deseilligny, C. H., Rivaud, S., Gaymard, B., & Agid, Y. (1991). Cortical control of reflexive visually-guided saccades. Brain, 114(3), 1473-1485.

Plaisted, K., O'Riordan, M., & Baron-Cohen, S. (1998). Enhanced discrimination of novel, highly similar stimuli by adults with autism during a perceptual learning task. Journal of Child Psychology and Psychiatry, 39(5), 765-775.

Posner, M., Rothbart, M., & Voelker, P. (2016). Developing brain networks of attention. Current Opinion Pediatrics, 28(6), 720-724.

Posner, M. I., Walker, J. A., Friedrich, F. J., & Rafal, R. D. (1984). Effects of parietal injury on covert orienting of attention. Neuroscience, 4(7), 1863-1874.

Remington, A., Swettenham, J., Campbell, R., & Coleman, M. (2009). Selective attention and perceptual load in autism spectrum disorder. Psychological Science, 20(11), 1388-1393.

Robertson, C. E., Kravitz, D. J., Freyberg, J., Baron-Cohen, S., & Baker, C. I. (2013). Tunnel vision:Sharper gradient of spatial attention in autism. Neuroscience, 33(16), 6776-6781.

Rueda, M. R., Pozuelos, J. P., & Cómbita, L. M. (2015). Cognitive neuroscience of attention from brain mechanisms to individual differences in efficiency. AIMS Neuroscience, 2(4), 183-202.

Sacrey, L.-A. R., Armstrong, V. L., Bryson, S. E., & Zwaigenbaum, L. (2014). Impairments to visual disengagement in autism spectrum disorder:A review of experimental studies from infancy to adulthood. Neuroscience and Biobehavioral Reviews, 47, 559-577.

Sasson, N. J., & Touchstone, E. W. (2014). Visual attention to competing social and object images by preschool children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 44(3), 584-592.

Schmitt, L. M., Cook, E. H., Sweeney, J. A., & Mosconi, M. W. (2014). Saccadic eye movement abnormalities in autism spectrum disorder indicate dysfunctions in cerebellum and brainstem. Molecular Autism, 5(1), 47.

Schoen, S. A., Miller, L. J., Brett-Green, B., & Hepburn, S. L. (2008). Psychophysiology of children with autism spectrum disorder. Research in Autism Spectrum Disorders, 2(3), 417-429.

Shirama, A., Kato, N., & Kashino, M. (2017). When do individuals with autism spectrum disorder show superiority in visual search? Autism, 21(8), 942-951.

Simmons, D. R., Robertson, A. E., McKay, L. S., Toal, E., McAleer, P., & Pollick, F. E. (2009). Vision in autism spectrum disorders. Vision Research, 49(22), 2705-2739.

Song, Y. N, Hakoda, Y. J., Sanefuji, W., & Cheng, C. (2015). Can they see it? The functional field of view is narrower in individuals with autism spectrum disorder. Plos One, 10(7), e0133237.

Takarae, Y., Minshew, N. J., Luna, B., & Sweeney, J. A. (2004). Oculomotor abnormalities parallel cerebellar histopathology in autism. Journal of Neurology Neurosurgery and Psychiatry, 75(9), 1359-1361.

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(3), 563-584.

Treisman, A. M. (1980). A feature-integration theory of attention. Cognitive Psychology, 12(1), 97-136.

Unruh, K. E., Sasson, N. J., Shafer, R. L., Whitten, A., Miller, S. J., Turner-Brown, L., & Bodfish, J. W. (2016). Social orienting and attention is influenced by the presence of competing nonsocial information in adolescents with autism. Frontiers in Neuroscience, 10, 586.

van der Hallen, R., Vanmarcke, S., Noens, I., & Wagemans, J. (2017). Hierarchical letters in ASD:High stimulus variability under different attentional modes. Journal of Autism and Developmental Disorders, 47(6), 1854-1865.

Velasquez, F., Qin, X. A., Reilly, M. A., Neuhaus, E., Estes, A., Aylward, E., & Kleinhans, N. M. (2017). Neural correlates of emotional inhibitory control in autism spectrum disorders. Research in Developmental Disabilities, 64, 64-77.

Vivanti, G., Fanning, P. A. J., Hocking, D. R., Sievers, S., & Dissanayake, C. (2017). Social attention, joint attention and sustained attention in autism spectrum disorder and williams syndrome:Convergences and divergences. Journal of Autism and Developmental Disorders, 47(6), 1866-1877.

Vossel, S., Weidner, R., Moos, K., & Fink, G. R. (2016). Individual attentional selection capacities are reflected in interhemispheric connectivity of the parietal cortex. Neuroimage, 129, 148-158.

Wu, X., & Fu, S. M. (2017). The different roles of category-and feature-specific attentional control settings on attentional enhancement and inhibition. Attention Perception & Psychophysics, 79(7), 1968-1978.

Wu, X., Liu, X. Y., & Fu, S. M. (2016). Feature-and category-specific attentional control settings are differently affected by attentional engagement in contingent attentional capture. Biological Psychology, 118, 8-16.

Zalla, T., Seassau, M., Cazalis, F., Gras, D., & Leboyer, M. (2018). Saccadic eye movements in adults with high-functioning autism spectrum disorder. Autism, 22(2), 195-204.

Zwaigenbaum, L., Bryson, S., Rogers, T., Roberts, W., Brian, J., & Szatmari, P. (2005). Behavioral manifestations of autism in the first year of life. International Journal of Developmental Neuroscience, 23(2-3), 143-152.