No rapid audiovisual recalibration in adults on the autism spectrum

Scientific Reports - Tập 6 Số 1
Marco Turi1, Themelis Karaminis2, Elizabeth Pellicano2, David C. Burr3
1Department of Translational Research On New Technologies in Medicine and Surgery, University of Pisa,
2Centre for Research in Autism and Education (CRAE), UCL Institute of Education, University College London, UK
3Department of Neuroscience, Psychology, Pharmacology and Child Health, University of Florence, Italy

Tóm tắt

Abstract

Autism spectrum disorders (ASD) are characterized by difficulties in social cognition, but are also associated with atypicalities in sensory and perceptual processing. Several groups have reported that autistic individuals show reduced integration of socially relevant audiovisual signals, which may contribute to the higher-order social and cognitive difficulties observed in autism. Here we use a newly devised technique to study instantaneous adaptation to audiovisual asynchrony in autism. Autistic and typical participants were presented with sequences of brief visual and auditory stimuli, varying in asynchrony over a wide range, from 512 ms auditory-lead to 512 ms auditory-lag and judged whether they seemed to be synchronous. Typical adults showed strong adaptation effects, with trials proceeded by an auditory-lead needing more auditory-lead to seem simultaneous and vice versa. However, autistic observers showed little or no adaptation, although their simultaneity curves were as narrow as the typical adults. This result supports recent Bayesian models that predict reduced adaptation effects in autism. As rapid audiovisual recalibration may be fundamental for the optimisation of speech comprehension, recalibration problems could render language processing more difficult in autistic individuals, hindering social communication.

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Tài liệu tham khảo

American Psychiatric Association Arlington, V. A. P. P. Diagnostic and statistical manual of mental disorders (5th ed.) (2013).

Bagby, M. S., Dickie, V. A. & Baranek, G. T. How Sensory Experiences of Children With and Without Autism Affect Family Occupations. American Journal of Occupational Therapy 66, 78–86, doi: 10.5014/Ajot.2012.000604 (2012).

Williams, D. Somebody somewhere: breaking free from the world of autism. 1st edn, (Times Book, 1994).

Sumby, W. H. & Pollack, I. Visual Contribution to Speech Intelligibility in Noise. The Journal of the Acoustical Society of America 26, 212–215, doi: 10.1121/1.1907309 (1954).

King, A. J. & Palmer, A. R. Integration of visual and auditory information in bimodal neurones in the guinea-pig superior colliculus. Exp Brain Res 60, 492–500 (1985).

Fujisaki, W., Shimojo, S., Kashino, M. & Nishida, S. Recalibration of audiovisual simultaneity. Nat Neurosci 7, 773–778, doi: 10.1038/nn1268 (2004).

Navarra, J., Hartcher-O’Brien, J., Piazza, E. & Spence, C. Adaptation to audiovisual asynchrony modulates the speeded detection of sound. Proc Natl Acad Sci USA 106, 9169–9173, doi: 10.1073/pnas.0810486106 (2009).

Roseboom, W. & Arnold, D. H. Twice upon a time: multiple concurrent temporal recalibrations of audiovisual speech. Psychol Sci 22, 872–877, doi: 10.1177/0956797611413293 (2011).

Vroomen, J., Keetels, M., de Gelder, B. & Bertelson, P. Recalibration of temporal order perception by exposure to audio-visual asynchrony. Brain Res Cogn Brain Res 22, 32–35, doi: 10.1016/j.cogbrainres.2004.07.003 (2004).

Van der Burg, E., Alais, D. & Cass, J. Rapid recalibration to audiovisual asynchrony. J Neurosci 33, 14633–14637, doi: 10.1523/JNEUROSCI.1182-13.2013 (2013).

Van der Burg, E. & Goodbourn, P. T. Rapid, generalized adaptation to asynchronous audiovisual speech. Proc Biol Sci 282, 20143083, doi: 10.1098/rspb.2014.3083 (2015).

Wozny, D. R. & Shams, L. Recalibration of auditory space following milliseconds of cross-modal discrepancy. J Neurosci 31, 4607–4612, doi: 10.1523/JNEUROSCI.6079-10.2011 (2011).

Bebko, J. M., Weiss, J. A., Demark, J. L. & Gomez, P. Discrimination of temporal synchrony in intermodal events by children with autism and children with developmental disabilities without autism. J Child Psychol Psychiatry 47, 88–98, doi: 10.1111/j.1469-7610.2005.01443.x (2006).

Charbonneau, G. et al. Multilevel alterations in the processing of audio–visual emotion expressions in autism spectrum disorders. Neuropsychologia 51, 1002–1010, doi: 10.1016/j.neuropsychologia.2013.02.009 (2013).

Gelder, B. d., Vroomen, J. & van der Heide, L. Face recognition and lip-reading in autism. European Journal of Cognitive Psychology 3, 69–86, doi: 10.1080/09541449108406220 (1991).

Magnée, M. J. C. M., De Gelder, B., Van Engeland, H. & Kemner, C. Audiovisual speech integration in pervasive developmental disorder: evidence from event-related potentials. Journal of Child Psychology and Psychiatry 49, 995–1000, doi: 10.1111/j.1469-7610.2008.01902.x (2008).

Megnin, O. et al. Audiovisual speech integration in autism spectrum disorders: ERP evidence for atypicalities in lexical-semantic processing. Autism Res 5, 39–48, doi: 10.1002/aur.231 (2012).

Mongillo, E. A. et al. Audiovisual processing in children with and without autism spectrum disorders. J Autism Dev Disord 38, 1349–1358, doi: 10.1007/s10803-007-0521-y (2008).

Smith, E. G. & Bennetto, L. Audiovisual speech integration and lipreading in autism. Journal of Child Psychology and Psychiatry 48, 813–821, doi: 10.1111/j.1469-7610.2007.01766.x (2007).

de Boer-Schellekens, L., Eussen, M. & Vroomen, J. Diminished sensitivity of audiovisual temporal order in autism spectrum disorder. Frontiers in Integrative Neuroscience 7, 8, doi: 10.3389/fnint.2013.00008 (2013).

Foss-Feig, J. H. et al. An extended multisensory temporal binding window in autism spectrum disorders. Exp Brain Res 203, 381–389, doi: 10.1007/s00221-010-2240-4 (2010).

Kwakye, L. D., Foss-Feig, J. H., Cascio, C. J., Stone, W. L. & Wallace, M. T. Altered auditory and multisensory temporal processing in autism spectrum disorders. Front Integr Neurosci 4, 129, doi: 10.3389/fnint.2010.00129 (2011).

Stevenson, R. A. et al. Multisensory temporal integration in autism spectrum disorders. J Neurosci 34, 691–697, doi: 10.1523/JNEUROSCI.3615-13.2014 (2014).

Collignon, O. et al. Reduced multisensory facilitation in persons with autism. Cortex 49, 1704–1710, doi: 10.1016/j.cortex.2012.06.001 (2013).

Pellicano, E. & Burr, D. When the world becomes ‘too real’: a Bayesian explanation of autistic perception. Trends Cogn Sci 16, 504–510, doi: 10.1016/j.tics.2012.08.009 (2012).

Kersten, D., Mamassian, P. & Yuille, A. Object perception as Bayesian inference. Annual review of psychology 55, 271–304, doi: 10.1146/annurev.psych.55.090902.142005 (2004).

Knill, D. C. & Pouget, A. The Bayesian brain: the role of uncertainty in neural coding and computation. Trends in neurosciences 27, 712–719, doi: 10.1016/j.tins.2004.10.007 (2004).

Mamassian, P., Landy, M. & Maloney, L. In Probabilistic Models of the Brain: Perception and Neural Function (eds R. Rao, B. Olshausen, & M. Lewicki ) (Bradford Books, 2002).

Friston, K. J., Lawson, R. & Frith, C. D. On hyperpriors and hypopriors: comment on Pellicano and Burr. Trends Cogn Sci 17, 1, doi: 10.1016/j.tics.2012.11.003 (2013).

Lawson, R. P., Rees, G. & Friston, K. J. An aberrant precision account of autism. Frontiers in Human Neuroscience 8, doi: 10.3389/fnhum.2014.00302 (2014).

Van de Cruys, S., de-Wit, L., Evers, K., Boets, B. & Wagemans, J. Weak priors versus overfitting of predictions in autism: Reply to Pellicano and Burr (TICS, 2012). Iperception 4, 95–97, doi: 10.1068/i0580ic (2013).

Sinha, P. et al. Autism as a disorder of prediction. Proceedings of the National Academy of Sciences 111, 15220–15225, doi: 10.1073/pnas.1416797111 (2014).

Rosenberg, A., Patterson, J. S. & Angelaki, D. E. A computational perspective on autism. Proceedings of the National Academy of Sciences 112, 9158–9165, doi: 10.1073/pnas.1510583112 (2015).

Pellicano, E., Jeffery, L., Burr, D. & Rhodes, G. Abnormal adaptive face-coding mechanisms in children with autism spectrum disorder. Curr Biol 17, 1508–1512, doi: 10.1016/j.cub.2007.07.065 (2007).

Turi, M. et al. Children with autism spectrum disorder show reduced adaptation to number. Proc Natl Acad Sci U S A 112, 7868–7872, doi: 10.1073/pnas.1504099112 (2015).

Barlow, H. Conditions for versatile learning, Helmholtz’s unconscious inference and the task of perception. Vision Res 30, 1561–1571 (1990).

Clifford, C. W. et al. Visual adaptation: neural, psychological and computational aspects. Vision Res 47, 3125–3131, doi: 10.1016/j.visres.2007.08.023 (2007).

Webster M. A. W. J. Field DJ Oxford, UK: Oxford University Press. pp. 241–277. In Advances in Cognition Series: Vol.2. Fitting the Mind to the World: Adaptation and Aftereffects in High Level Vision. (ed Clifford, C. & Rhodes, G. ) (Oxford University Press, 2005).

Chopin, A. & Mamassian, P. Predictive properties of visual adaptation. Curr Biol 22, 622–626, doi: 10.1016/j.cub.2012.02.021 (2012).

Stocker, A. A. & Simoncelli, E. P. Sensory adaptation within a Bayesian framework for perception. In Y. Weiss, B. Schoelkopf, & J. Platt (Eds.). Advance in neural information processing systems. (2006).

Pellicano, E., Rhodes, G., Jeffery, L. & Burr, D. Children with autism spectrum disorder show typical adaptation to motion. Manuscript in preparation (2015).

Karaminis, T. et al. Atypicalities in Perceptual Adaptation in Autism Do Not Extend to Perceptual Causality. PLoS ONE 10, e0120439, doi: 10.1371/journal.pone.0120439 (2015).

Lawson, R. P., Aylward, J., White, S. & Rees, G. A striking reduction of simple loudness adaptation in autism. Sci Rep 5, 16157, doi: 10.1038/srep16157 (2015).

Clifford, C. W. G. & Rhodes, G. Fitting the mind to the world: adaptation and after-effects in high-level vision. 1st edn, (Oxford University Press, 2005).

Rhodes, G. & Jeffery, L. Adaptive norm-based coding of facial identity. Vision Res 46, 2977–2987, doi: 10.1016/j.visres.2006.03.002 (2006).

Van der Burg, E., Orchard-Mills, E. & Alais, D. Rapid temporal recalibration is unique to audiovisual stimuli. Exp Brain Res 233, 53–59, doi: 10.1007/s00221-014-4085-8 (2015).

Lord, C. et al. Autism Diagnostic Observation Schedule, Second Edition (ADOS-2). (Western Psychological Services, 2012).

Constantino, J. N. G. C. P. Social Responsiveness Scale, Second Edition. (Western Psychological Services, 2012).

Brainard, D. H. The Psychophysics Toolbox. Spat Vis 10, 433–436 (1997).

Wechsler, D. Wechsler Abbreviated Scale of Intelligence. (The Psychological Corporation: Harcourt Brace & Company, 1999).