Visual Attention in Autism Families: ‘Unaffected’ Sibs Share Atypical Frontal Activation

Matthew K Belmonte
Marie Gomot
Simon Baron-Cohen

Journal of Child Psychology and Psychiatry 51(3):259-276 (March 2010).

The definitive version is available at www.blackwell-synergy.com.


ABSTRACT

Background: In addition to their more clinically evident abnormalities of social cognition, people with autism spectrum conditions (ASC) manifest perturbations of attention and sensory perception which may offer insights into the underlying neural abnormalities. Similar autistic traits in ASC relatives without a diagnosis suggest a continuity between clinically affected and unaffected family members. Methods: We applied fMRI in the context of a non-social task of visual attention in order to determine whether this continuity persists at the level of brain physiology. Results: Both boys with ASC and clinically unaffected brothers of people with ASC were impaired at a visual divided-attention task demanding conjunction of attributes from rapidly and simultaneously presented, spatially disjoint stimuli and suppression of spatially intervening distractors. In addition, both groups in comparison to controls manifested atypical fronto-cerebellar activation as a function of distractor congruence, and the degree of this frontal atypicality correlated with psychometric measures of autistic traits in ASC and sibs. Despite these resemblances between the ASC and sib groups, an exploratory, hypothesis-generating analysis of correlations across brain regions revealed a decrease in overall functional correlation only in the ASC group and not in the sibs. Conclusions: These results establish a neurophysiological correlate of familial susceptibility to ASC, and suggest that whilst abnormal time courses of frontal activation may reflect processes permissive of autistic brain development, abnormal patterns of functional correlation across a wider array of brain regions may relate more closely to autism’s determinants.


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CITED IN PUBLICATIONS BY OTHERS:

  1. Boso M, Emanuele E, Prestori F, Politi P, Barale F, D'Angelo E. Autism and genius: Is there a link? The involvement of central brain loops and hypotheses for functional testing. Functional Neurology 25(1):27-32 (January-March 2010).
  2. Elsabbagh M, Johnson MH. Getting answers from babies about autism. Trends in Cognitive Sciences 14(2):81-87 (February 2010).
  3. Kaiser MD, Hudac CM, Shultz S, Lee SM, Cheung C, Berken AM, Deen B, Pitskel NB, Sugrue DR, Voos AC, Saulnier CA, Ventola P, Wolf JM, Klin A, Vander Wyk BC, Pelphrey KA. Neural signatures of autism. Proceedings of the National Academy of Sciences of the United States of America 107(49):21223-21228 (7 December 2010).
  4. Koh HC, Milne E, Dobkins K. Contrast sensitivity for motion detection and direction discrimination in adolescents with autism spectrum disorders and their siblings. Neuropsychologia 48(14):4046-4056 (December 2010).
  5. Markram K, Markram H. The intense world theory - a unifying theory of the neurobiology of autism. Frontiers in Human Neuroscience 4:224 (21 December 2010).
  6. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O’Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P, Deisseroth K. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477(7363):171-178 (8 September 2011).
  7. Anderson JS, Nielsen JA, Froehlich AL, DuBray MB, Druzgal TJ, Cariello AN, Cooperrider JR, Zielinski BA, Ravichandran C, Fletcher PT, Alexander AL, Bigler ED, Lange N, Lainhart JE. Functional connectivity magnetic resonance imaging classification of autism. Brain 134(12):3739-3751 (December 2011).
  8. Sucksmith E, Roth I, Hoekstra RA. Autistic traits below the clinical threshold: re-examining the broader autism phenotype in the 21st century. Neuropsychology Review 21(4):360-389 (December 2011).
  9. Lintas C, Sacco R, Persico AM. Genome-wide expression studies in autism spectrum disorder, Rett syndrome, and Down syndrome. Neurobiology of Disease 45(1):57-68 (January 2012).
  10. Yizhar O. Optogenetic insights into social behavior function. Biological Psychiatry 71(12):1075-1080 (15 June 2012).
  11. Pina-Camacho L, Villero S, Fraguas D, Boada L, Janssen J, Navas-Sanchez FJ, Mayoral M, Llorente C, Arango C, Parellada M. Autism spectrum disorder: does neuroimaging support the dsm-5 proposal for a symptom dyad? A systematic review of functional magnetic resonance imaging and diffusion tensor imaging studies. Journal of Autism and Developmental Disorders 42(7):1326-1341 (July 2012).
  12. Ohta H, Yamada T, Watanabe H, Kanai C, Tanaka E, Ohno T, Takayama Y, Iwanami A, Kato N, Hashimoto R. An fMRI study of reduced perceptual load-dependent modulation of task-irrelevant activity in adults with autism spectrum conditions. NeuroImage 61(4):1176-1187 (16 July 2012).
  13. McFadden KL, Hepburn S, Winterrowd E, Schmidt GL, Rojas DC. Abnormalities in gamma-band responses to language stimuli in first-degree relatives of children with autism spectrum disorder: an MEG study. BMC Psychiatry 12:213 (29 November 2012).

CITED IN MY OTHER PUBLICATIONS:

  1. Belmonte MK. What’s the story behind ‘theory of mind’ and autism? Journal of Consciousness Studies 16(6-8):118-139 (June-August 2009).