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Cited by 17Autism Spectrum Disorder ResearchAction Observation and SynchronizationFace Recognition and Perception

Recognizing visual speech: Reduced responses in visual-movement regions, but not other speech regions in autism

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Borowiak, Kamila, Schelinski, Stefanie, von Kriegstein, Katharina·2018·NeuroImage: Clinical
DOI 10.1016/j.nicl.2018.09.019PMC PMC6202694
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Abstract

Speech information inherent in face movements is important for understanding what is said in face-to-face communication. Individuals with autism spectrum disorders (ASD) have difficulties in extracting speech information from face movements, a process called visual-speech recognition. Currently, it is unknown what dysfunctional brain regions or networks underlie the visual-speech recognition deficit in ASD. We conducted a functional magnetic resonance imaging (fMRI) study with concurrent eye tracking to investigate visual-speech recognition in adults diagnosed with high-functioning autism and pairwise matched typically developed controls. Compared to the control group (n = 17), the ASD group (n = 17) showed decreased Blood Oxygenation Level Dependent (BOLD) response during visual-speech recognition in the right visual area 5 (V5/MT) and left temporal visual speech area (TVSA) - brain regions implicated in visual-movement perception. The right V5/MT showed positive correlation with visual-speech task performance in the ASD group, but not in the control group. Psychophysiological interaction analysis (PPI) revealed that functional connectivity between the left TVSA and the bilateral V5/MT and between the right V5/MT and the left IFG was lower in the ASD than in the control group. In contrast, responses in other speech-motor regions and their connectivity were on the neurotypical level. Reduced responses and network connectivity of the visual-movement regions in conjunction with intact speech-related mechanisms indicate that perceptual mechanisms might be at the core of the visual-speech recognition deficit in ASD. Communication deficits in ASD might at least partly stem from atypical sensory processing and not higher-order cognitive processing of socially relevant information.

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  1. Alaerts K. Woolley D.G. Steyaert J. Di Martino A. Swinnen S.P. Wenderoth N. Underconnectivity of the superior temporal sulcus predicts emotion recognition deficits in autism Soc. Cogn. Affect. Neurosci. 9 2013 1589 1600 24078018 PMC4187281
  2. Alaerts K. Swinnen S.P. Wenderoth N. Neural processing of biological motion in autism: an investigation of brain activity and effective connectivity Sci. Rep. 7 2017 PMC5514051 28717158
  3. Allison T. Puce A. McCarthy G. Social perception from visual cues: role of the STS region Trends Cogn. Sci. 4 2000 267 278 10859571
  4. Ashwood K.L. Gillan N. Horder J. Hayward H. Woodhouse E. McEwen F.S. Findon J. Eklund H. Spain D. Wilson C.E. Cadman T. Predicting the diagnosis of autism in adults using the Autism-Spectrum Quotient (AQ) questionnaire Psychol. Med. 46 2016 2595 2604 27353452 PMC4988267
  5. Baron-Cohen S. Mindblindness: An Essay on Autism and Theory of Mind 1997 MIT press
  6. Baron-Cohen S. Wheelwright S. Skinner R. Martin J. Clubley E. Evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians J. Autism Dev. Disord. 31 2001 5 17 The autism-spectrum quotient (AQ) 11439754
  7. Beckers G. Homberg V. Cerebral visual motion blindness: transitory akinetopsia induced by transcranial magnetic stimulation of human area V5 Proc. R. Soc. Lond. B Biol. Sci. 249 1992 173 178 1360678
  8. Bernstein M. Yovel G. Two neural pathways of face processing: a critical evaluation of current models Neurosci. Biobehav. Rev. 55 2015 536 546 26067903
  9. Bernstein L.E. Jiang J. Pantazis D. Lu Z.L. Joshi A. Visual phonetic processing localized using speech and nonspeech face gestures in video and point-light displays Hum. Brain Mapp. 32 2011 1660 1676 20853377 PMC3120928
  10. Blank H. von Kriegstein K. Mechanisms of enhancing visual-speech recognition by prior auditory information NeuroImage 65 2013 109 118 23023154
  11. Boddaert N. Belin P. Chabane N. Poline J.B. Barthélémy C. Mouren-Simeoni M.C. Brunelle F. Samson Y. Zilbovicius M. Perception of complex sounds: abnormal pattern of cortical activation in autism Am. J. Psychiatry 160 2003 2057 2060 14594758
  12. Brieber S. Herpertz-Dahlmann B. Fink G.R. Kamp-Becker I. Remschmidt H. Konrad K. Coherent motion processing in autism spectrum disorder (ASD) an fMRI study Neuropsychologia 48 2010 1644 1651 20153764
  13. Callan D.E. Jones J.A. Callan A. Multisensory and modality specific processing of visual speech in different regions of the premotor cortex Front. Psychol. 5 2014 PMC4017150 24860526
  14. Calvert G.A. Campbell R. Reading speech from still and moving faces: the neural substrates of visible speech J. Cogn. Neurosci. 15 2003 57 70 12590843
  15. Calvert G.A. Bullmore E.T. Brammer M.J. Campbell R. Williams S.C. McGuire P.K. Woodruff P.W.R. Iversen S. David A.S. Activation of auditory cortex during silent lipreading Science 276 1997 593 596 9110978
  16. Campbell R. MacSweeney M. Surguladze S. Calvert G. McGuire P. Suckling J. Brammer M.J. David A.S. Cortical substrates for the perception of face actions: an fMRI study of the specificity of activation for seen speech and for meaningless lower-face acts (gurning) Cogn. Brain Res. 12 2001 233 243 11587893
  17. Cauda F. Costa T. Palermo S. D'Agata F. Diano M. Bianco F. Duca S. Keller R. Concordance of white matter and gray matter abnormalities in autism spectrum disorders: a voxel-based meta-analysis study Hum. Brain Mapp. 35 2014 2073 2098 23894001 PMC6869166
  18. Chu Y.H. Lin F.H. Chou Y.J. Tsai K.W.K. Kuo W.J. Jääskeläinen I.P. Effective cerebral connectivity during silent speech reading revealed by functional magnetic resonance imaging PLoS One 8 2013 e80265 PMC3837007 24278266
  19. DeRamus T.P. Kana R.K. Anatomical likelihood estimation meta-analysis of grey and white matter anomalies in autism spectrum disorders Neuroimage Clin. 7 2015 525 536 25844306 PMC4375647
  20. Desikan R.S. Ségonne F. Fischl B. Quinn B.T. Dickerson B.C. Blacker D. Buckner R.L. Dale A.M. Maguire R.P. Hyman B.T. Albert M.S. Killiany R.J. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest NeuroImage 31 2006 968 980 16530430
  21. Eickhoff S.B. Paus T. Caspers S. Grosbras M.H. Evans A.C. Zilles K. Amunts K. Assignment of functional activations to probabilistic cytoarchitectonic areas revisited NeuroImage 36 2007 511 521 17499520
  22. Ethofer T. Gschwind M. Vuilleumier P. Processing social aspects of human gaze: a combined fMRI-DTI study NeuroImage 55 2011 411 419 21095230
  23. Foxe J.J. Molholm S. Del Bene V.A. Frey H.P. Russo N.N. Blanco D. Saint-Amour D. Ross L.A. Severe multisensory speech integration deficits in high-functioning school-aged children with autism spectrum disorder (ASD) and their resolution during early adolescence Cereb. Cortex 25 2015 298 312 23985136 PMC4303800
  24. Freitag C.M. Konrad C. Häberlen M. Kleser C. von Gontard A. Reith W. Troje N.F. Krick C. Perception of biological motion in autism spectrum disorders Neuropsychologia 46 2008 1480 1494 18262208
  25. Friston K.J. Buechel C. Fink G.R. Morris J. Rolls E. Dolan R.J. Psychophysiological and modulatory interactions in neuroimaging NeuroImage 6 1997 218 229 9344826
  26. Friston K.J. Ashburner A. Kiebel S. Nichols T. Penny W. Statistical Parametric Mapping, The Analysis of Functional Brain Images 2007 Academic Press
  27. Furl N. Henson R.N. Friston K.J. Calder A.J. Network interactions explain sensitivity to dynamic faces in the superior temporal sulcus Cereb. Cortex 25 2014 2876 2882 24770707 PMC4537434
  28. Giraud A.L. Price C.J. Graham J.M. Truy E. Frackowiak R.S. Cross-modal plasticity underpins language recovery after cochlear implantation Neuron 30 2001 657 664 11430800
  29. Grèzes J. Fonlupt P. Bertenthal B. Delon-Martin C. Segebarth C. Decety J. Does perception of biological motion rely on specific brain regions? NeuroImage 13 2001 775 785 11304074
  30. Grossman E.D. Battelli L. Pascual-Leone A. Repetitive TMS over posterior STS disrupts perception of biological motion Vis. Res. 45 2005 2847 2853 16039692
  31. Hall D.A. Fussell C. Summerfield A.Q. Reading fluent speech from talking faces: typical brain networks and individual differences J. Cogn. Neurosci. 17 2005 939 953 15969911
  32. Ioannidis J.P. Why most published research findings are false PLoS Med. 2 2005 e124 PMC1182327 16060722
  33. Irwin J.R. Brancazio L. Seeing to hear? Patterns of gaze to speaking faces in children with autism spectrum disorders Front. Psychol. 5 2014 PMC4021198 24847297
  34. Irwin J.R. Tornatore L.A. Brancazio L. Whalen D.H. Can children with autism spectrum disorders “hear” a speaking face? Child Dev. 82 2011 1397 1403 21790542 PMC3169706
  35. Jezzard P. Balaban R.S. Correction for geometric distortion in echo planar images from B0 field variations Magn. Reson. Med. 34 1995 65 73 7674900
  36. Jiang J. Borowiak K. Tudge L. Otto C. von Kriegstein K. Neural mechanisms of eye contact when listening to another person talking Soc. Cogn. Affect. Neurosci. 12 2017 319 328 27576745 PMC5390711
  37. Koldewyn K. Whitney D. Rivera S.M. Neural correlates of coherent and biological motion perception in autism Dev. Sci. 14 2011 1075 1088 21884323 PMC3800149
  38. von Kriegstein K. Dogan Ö. Grüter M. Giraud A.L. Kell C.A. Grüter T. Kleinschmidt A. Kiebel S.J. Simulation of talking faces in the human brain improves auditory speech recognition Proc. Natl. Acad. Sci. 105 2008 6747 6752 18436648 PMC2365564
  39. Lee H.J. Truy E. Mamou G. Sappey-Marinier D. Giraud A.L. Visual speech circuits in profound acquired deafness: a possible role for latent multimodal connectivity Brain 130 2007 2929 2941 17906328
  40. Lord C. Rutter M. Le Couteur A. Autism Diagnostic Interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders J. Autism Dev. Disord. 24 1994 659 685 7814313
  41. Lord C. Risi S. Lambrecht L. Cook E.H. Leventhal B.L. DiLavore P.C. Pickles A. Rutter M. The autism diagnostic observation schedule—Generic: a standard measure of social and communication deficits associated with the spectrum of autism J. Autism Dev. Disord. 30 2000 205 223 11055457
  42. Malikovic A. Amunts K. Schleicher A. Mohlberg H. Eickhoff S.B. Wilms M. Palomero-Gallagher N. Armstrong E. Zilles K. Cytoarchitectonic analysis of the human extrastriate cortex in the region of V5/MT+: a probabilistic, stereotaxic map of area hOc5 Cereb. Cortex 17 2007 562 574 16603710
  43. Marassa L.K. Lansing C.R. Visual word recognition in two facial motion conditions: full-face versus lips-plus-mandible J. Speech Lang. Hear. Res. 38 1995 1387 1394 8747830
  44. Nichols T. Hayasaka S. Controlling the familywise error rate in functional neuroimaging: a comparative review Stat. Methods Med. Res. 12 2003 419 446 14599004
  45. Nickl-Jockschat T. Habel U. Michel T.J. Manning J. Laird A.R. Fox P.T. Schneider F. Eickhoff S.B. Brain structure anomalies in autism spectrum disorder - a meta-analysis of VBM studies using anatomic likelihood estimation Hum. Brain Mapp. 33 2012 1470 1489 21692142 PMC4801488
  46. Nishitani N. Hari R. Viewing lip forms: cortical dynamics motor cortex, both during execution of hand actions Neuron 36 2002 1211 1220 12495633
  47. Okada K. Hickok G. Two cortical mechanisms support the integration of visual and auditory speech: a hypothesis and preliminary data Neurosci. Lett. 452 2009 219 223 19348727 PMC2667381
  48. Oldfield R.C. The assessment and analysis of handedness–he Edinburgh inventory Neuropsychologia 9 1971 97 113 5146491
  49. O'Toole A.J. Roark D.A. Abdi H. Recognizing moving faces: a psychological and neural synthesis Trends Cogn. Sci. 6 2002 261 266 12039608
  50. Pelphrey K.A. Morris J.P. McCarthy G. LaBar K.S. Perception of dynamic changes in facial affect and identity in autism Soc. Cogn. Affect. Neurosci. 2 2007 40 149 PMC2174259 18174910
  51. Puce A. Allison T. Bentin S. Gore J.C. McCarthy G. Temporal cortex activation in humans viewing eye and mouth movements J. Neurosci. 18 1998 2188 2199 9482803 PMC6792917
  52. Riedel P. Ragert P. Schelinski S. Kiebel S.J. von Kriegstein K. Visual face-movement sensitive cortex is relevant for auditory-only speech recognition Cortex 68 2015 86 99 25650106
  53. Robertson C.E. Baron-Cohen S. Sensory perception in autism Nat. Rev. Neurosci. 18 2017 671 684 28951611
  54. Robertson C.E. Martin A. Baker C.I. Baron-Cohen S. Atypical integration of motion signals in autism spectrum conditions PLoS One 7 2012 e48173 PMC3502435 23185249
  55. Robertson C.E. Thomas C. Kravitz D.J. Wallace G.L. Baron-Cohen S. Martin A. Baker C.I. Global motion perception deficits in autism are reflected as early as primary visual cortex Brain 137 2014 2588 2599 25060095 PMC4132651
  56. Ross L.A. Saint-Amour D. Leavitt V.M. Javitt D.C. Foxe J.J. Do you see what I am saying? Exploring visual enhancement of speech comprehension in noisy environments Cereb. Cortex 17 2007 1147 1153 16785256
  57. Rouger J. Lagleyre S. Fraysse B. Deneve S. Deguine O. Baron P. Evidence that cochlear-implanted deaf patients are better multisensory integrators Proc. Natl. Acad. Sci. 104 2007 7295 7300 17404220 PMC1855404
  58. Rühl D. Bölte S. Feineis-Matthews S. Poustka F. Diagnostische Beobachtungsskala für Autistische Störungen (ADOS) 2004 Verlag Hans Huber Bern 14992047
  59. Saalasti S. Kätsyri J. Tiippana K. Laine-Hernandez M. von Wendt L. Sams M. Audiovisual speech perception and eye gaze behavior of adults with Asperger syndrome J. Autism Dev. Disord. 42 2012 1606 1615 22068821
  60. Sato W. Toichi M. Uono S. Kochiyama T. Impaired social brain network for processing dynamic facial expressions in autism spectrum disorders BMC Neurosci. 13 2012 99 22889284 PMC3459703
  61. Schelinski S. Riedel P. von Kriegstein K. Visual abilities are important for auditory-only speech recognition: evidence from autism spectrum disorder Neuropsychologia 65 2014 1 11 25283605
  62. Skipper J.I. Nusbaum H.C. Small S.L. Listening to talking faces: motor cortical activation during speech perception NeuroImage 25 2005 76 89 15734345
  63. Smith E.G. Bennetto L. Audiovisual speech integration and lipreading in autism J. Child Psychol. Psychiatry 48 2007 813 821 17683453
  64. Smith S.M. Jenkinson M. Woolrich M.W. Beckmann C.F. Behrens T.E. Johansen-Berg H. Bannister P.R. De Luca M. Drobnjak I. Flitney D.E. Niazy R.K. Sunders J. Vickers J. Zhang Y. De Stefano N. Brady J.M. Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL NeuroImage 23 2004 S208 S219 15501092
  65. Travers B.G. Adluru N. Ennis C. Tromp D.P. Destiche D. Doran S. Bigler E.D. Lange N. Lainhart J.E. Alexander A.L. Diffusion tensor imaging in autism spectrum disorder: a review Autism Res. 5 2012 289 313 22786754 PMC3474893
  66. Tryfon A. Foster N.E. Sharda M. Hyde K.L. Speech perception in autism spectrum disorder: an activation likelihood estimation meta-analysis Behav. Brain Res. 338 2018 118 127 29074403
  67. Van der Hallen R. Evers K. Brewaeys K. Van den Noortgate W. Wagemans J. Global processing takes time: a meta-analysis on local–global visual processing in ASD Psychol. Bull. 141 2015 549 573 25420221
  68. Van Wassenhove V. Grant K.W. Poeppel D. Visual speech speeds up the neural processing of auditory speech Proc. Natl. Acad. Sci. U. S. A. 102 2005 1181 1186 15647358 PMC545853
  69. Wakabayashi A. Baron-Cohen S. Wheelwright S. Tojo Y. The Autism-Spectrum Quotient (AQ) in Japan: a cross-cultural comparison J. Autism Dev. Disord. 36 2006 263 270 16586157
  70. Watson J.D. Myers R. Frackowiak R.S. Hajna J.V. Woods R.P. Mazziotta J.C. Shipp S. Zeki S. Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging Cereb. Cortex 3 1993 79 94 8490322
  71. Williams J.H.G. Massaro D.W. Peel N.J. Bosseler A. Suddendorf T. Visual-auditory integration during speech imitation in autism Res. Dev. Disabil. 25 2004 559 575 15541632
  72. Wilson S.M. Saygin A.P. Sereno M.I. Iacoboni M. Listening to speech activates motor areas involved in speech production Nat. Neurosci. 7 2004 701 15184903
  73. Zeki S. Watson J.D. Lueck C.J. Friston K.J. Kennard C. Frackowiak R.S. A direct demonstration of functional specialization in human visual cortex J. Neurosci. 11 1991 641 649 2002358 PMC6575357

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Authors
Borowiak, K., Schelinski, S., & von Kriegstein, K.
Affiliations
  • Humboldt-Universität zu Berlin (DE)
  • Max Planck Institute for Human Cognitive and Brain Sciences (DE)
Corresponding author
Borowiak, Kamila
ORCID
Venue
NeuroImage: Clinical
Publisher
Elsevier BV
Published
2018
Volume
20
Pages
1078-1091
ISSN
2213-1582 (ISSN-L)
DOI
10.1016/j.nicl.2018.09.019
PMC
PMC6202694
OpenAlex
W2893020025
Cited by
17
References
5
Citations by year
2025: 1 · 2024: 3 · 2023: 4 · 2022: 2 · 2021: 4 · 2020: 1 · 2019: 2
FWCI
1.04
Type
journal article
Language
en
Open access
Licence
Locations
  • NeuroImage Clinical (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders
Technische Universität Dresden
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
  • Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
Keywords
visual speech recognition, autism spectrum disorder, high-functioning autism, MT/V5, functional connectivity, inferior frontal gyrus, perceptual deficits, face-to-face communication
MeSH terms
Autism Spectrum Disorder, Adult, Autistic Disorder, Brain, Brain Mapping, Female, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Motion Perception, Speech, Visual Perception, Recognition, Psychology, Young Adult

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