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Journal of Neurodevelopmental Disorders
Published in: Journal of Neurodevelopmental Disorders 1/2018

Open Access 01-12-2018 | Research

Neurophysiological correlates of holistic face processing in adolescents with and without autism spectrum disorder

Authors: Sandra Naumann, Ulrike Senftleben, Megha Santhosh, James McPartland, Sara Jane Webb

Published in: Journal of Neurodevelopmental Disorders | Issue 1/2018

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Abstract

Background

Face processing has been found to be impaired in autism spectrum disorders (ASD). One hypothesis is that individuals with ASD engage in piecemeal compared to holistic face processing strategies. To investigate the role of possible impairments in holistic face processing in individuals with autism, the current study investigated behavioral and electroencephalography (EEG) correlates of face processing (P1/N170 and gamma-band activity) in adolescents with ASD and sex-, age-, and IQ-matched neurotypical controls.

Methods

Participants were presented with upright and inverted Mooney stimuli; black and white low information faces that are only perceived as faces when processed holistically. Participants indicated behaviorally the detection of a face. EEG was collected time-locked to the presentation of the stimuli.

Results

Adolescents with ASD perceived Mooney stimuli as faces suggesting ability to use holistic processing but displayed a lower face detection rate and slower response times. ERP components suggest slowed temporal processing of Mooney stimuli in the ASD compared to control group for P1 latency but no differences between groups for P1 amplitude and at the N170. Increases in gamma-band activity was similar during the perception of the Mooney images by group, but the ASD group showed prolonged temporal elevation in activity.

Conclusion

Overall, our results suggest that adolescents with ASD were able to utilize holistic processing to perceive a face within the Mooney stimuli. Delays in early processing, marked by the P1, and elongated elevation in gamma activity indicate that the neural systems supporting holistic processing are slightly altered suggesting a less automatic and less efficient facial processing system.

Trial registration

Non-applicable.
Appendix
Available only for authorised users
Literature
1.
Jemel B, Mottron L, Dawson M. Impaired face processing in autism: fact or artifact? J Autism Dev Disord. 2006;36(1):91–106.CrossRefPubMed
2.
Webb SJ, Dawson G, Bernier R, Panagiotides H. ERP evidence of atypical face processing in young children with autism. J Autism Dev Disord. 2006;36(7):881–90.CrossRefPubMedPubMedCentral
3.
Taubert J, Apthorp D, Aagten-Murphy D, Alais D. The role of holistic processing in face perception: evidence from the face inversion effect. Vis Res. 2011;51(11):1273–8.CrossRefPubMed
4.
Zion-Golumbic E, Bentin S. Dissociated neural mechanisms for face detection and configural encoding: evidence from N170 and induced gamma-band oscillation effects. Cereb Cortex. 2007;17(8):1741–9.
5.
Freire A, Lee K, Symons LA. The face-inversion effect as a deficit in the encoding of Configural information: direct evidence. Perception. 2000;29(2):159–70.CrossRefPubMed
6.
Kumar SL. Examining the characteristics of Visuospatial information processing in individuals with high-functioning autism. Yale J Biol Med. 2013;86(2):147–56.PubMedPubMedCentral
7.
Piepers DW, Robbins RA. A review and clarification of the terms ‘holistic,’ ‘configural,’ and ‘relational’ in the face perception literature. Front Psychol. 2012;3:559.CrossRefPubMedPubMedCentral
8.
Steinberg Lowe M, Lewis GA, Poeppel D. Effects of part- and whole-object primes on early MEG responses to Mooney faces and houses. Front Psychol. 2016;7(February):147.PubMedPubMedCentral
9.
American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders (DSM-V), no. 1. 2013.CrossRef
10.
Joseph RM, Tanaka J. Holistic and part-based face recognition in children with autism. J Child Psychol Psychiatry Allied Discip. 2003;44(4):529–42.CrossRef
11.
D’Souza D, Booth R, Connolly M, Happé F, Karmiloff-Smith A. Rethinking the concepts of ‘local or global processors’: evidence from Williams syndrome, Down syndrome, and autism spectrum disorders. Dev Sci. 2016;19(3):452–68.CrossRefPubMed
12.
Webb SJ, Neuhaus E, Faja S. Face perception and learning in autism Spectrum disorders. Q J Exp Psychol. 2016;0218(May):1–44.
13.
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. 2015;141(3):549–73.CrossRefPubMed
14.
Frith U. Autism and ‘theory of mind. In: diagnosis and treatment of autism. New York: Plenum Press; 1989. p. 33–52.CrossRef
15.
Lahaie A, Mottron L, Arguin M, Berthiaume C, Jemel B, Saumier D. Face perception in high-functioning autistic adults: evidence for superior processing of face parts, not for a configural face-processing deficit. Neuropsychology. 2006;20(1):30–41.CrossRefPubMed
16.
Latinus M, Taylor MJ. Holistic processing of faces: learning effects with Mooney faces. J Cogn Neurosci. 2005;17(8):1316–27.CrossRefPubMed
17.
O’Connor K, Hamm JP, Kirk IJ. The neurophysiological correlates of face processing in adults and children with Asperger’s syndrome. Brain Cogn. 2005;59(1):82–95.CrossRefPubMed
18.
Rose FE, Lincoln AJ, Lai Z, Ene M, Searcy YM, Bellugi U. Orientation and affective expression effects on face recognition in Williams syndrome and autism. J Autism Dev Disord. 2007;37(3):513–22.CrossRefPubMed
19.
Sun L, et al. Impaired gamma-band activity during perceptual Organization in Adults with autism Spectrum disorders: evidence for dysfunctional network activity in frontal-posterior cortices. J Neurosci. 2012;32(28):9563–73.CrossRefPubMed
20.
Rutherford MD, Clements KA, Sekuler AB. Differences in discrimination of eye and mouth displacement in autism spectrum disorders. Vis Res. 2007;47(15):2099–110.CrossRefPubMed
21.
Scherf KS, Behrmann M, Minshew N, Luna B. Atypical development of face and greeble recognition in autism. J Child Psychol Psychiatry Allied Discip. 2008;49(8):838–47.CrossRef
22.
Weigelt S, Koldewyn K, Kanwisher N. Face identity recognition in autism spectrum disorders: a review of behavioral studies. Neurosci Biobehav Rev. 2012;36(3):1060–84.CrossRefPubMed
23.
McPartland J, Dawson G, Webb SJ, Panagiotides H, Carver LJ. Event-related brain potentials reveal anomalies in temporal processing of faces in autism spectrum disorder. J Child Psychol Psychiatry Allied Discip. 2004;45(7):1235–45.CrossRef
24.
Akechi H, Kikuchi Y, Tojo Y, Osanai H, Hasegawa T. Neural and behavioural responses to face-likeness of objects in adolescents with autism spectrum disorder. Sci Rep. 2014;4:1–7.
25.
George N, Jemel B, Fiori N, Chaby L, Renault B. Electrophysiological correlates of facial decision: insights from upright and upside-down Mooney-face perception. Cogn Brain Res. 2005;24(3):663–73.CrossRef
26.
Grützner C, Uhlhaas PJ, Genc E, Kohler A, Singer W, Wibral M. Neuroelectromagnetic correlates of perceptual closure processes. J Neurosci. 2010;30(24):8342–52.CrossRefPubMed
27.
Otsuka Y, Hill HCH, Kanazawa S, Yamaguchi MK, Spehar B. Perception of Mooney faces by young infants: the role of local feature visibility, contrast polarity, and motion. J Exp Child Psychol. 2012;111(2):164–79.CrossRefPubMed
28.
Verhallen RJ, Bosten JM, Goodbourn PT, Bargary G, Lawrance-Owen AJ, Mollon JD. An online version of the Mooney face test: phenotypic and genetic associations. Neuropsychologia. 2014;63(1):19–25.CrossRefPubMed
29.
Castelhano J, Rebola J, Leitão B, Rodriguez E, Castelo-Branco M. To perceive or not perceive: the role of gamma-band activity in signaling object percepts. PLoS One. 2013;8(6):35–7.CrossRef
30.
Gauthier I, Klaiman C, Schultz RT. Face composite effects reveal abnormal face processing in autism Spectrum disorders. Heal (San Fr.). 2010;49(4):470–8.
31.
Jeffery L, Taylor L, Rhodes G. Transfer of figural face aftereffects suggests mature orientation selectivity in 8-year-olds’ face coding. J Exp Child Psychol. 2014;126:229–44.CrossRefPubMed
32.
Taylor MJ, Batty M, Itier RJ. The faces of development: a review of early face processing over childhood. J Cogn Neurosci. 2004;16(8):1426–42.CrossRefPubMed
33.
Dawson G, Webb SJ, McPartland J. Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev Neuropsychol. 2005;27(3):403–24.CrossRefPubMed
34.
Jeste SS, Nelson CA. Event related potentials in the understanding of autism spectrum disorders: an analytical review. J Autism Dev Disord. 2009;39(3):495–510.CrossRefPubMed
35.
36.
Jacques C, Rossion B. Electrophysiological evidence for temporal dissociation between spatial attention and sensory competition during human face processing. Cereb Cortex. 2007;17(5):1055–65.CrossRefPubMed
37.
Neuhaus E, Kresse A, Faja S, Bernier RA, Webb SJ. Face processing among twins with and without autism: social correlates and twin concordance. Soc Cogn Affect Neurosci. 2016;11(1):44–54.CrossRefPubMed
38.
Webb SJ, Merkle K, Murias M, Richards T, Aylward E, Dawson G. ERP responses differentiate inverted but not upright face processing in adults with ASD. Soc Cogn Affect Neurosci. 2012;7(5):578–87.CrossRefPubMed
39.
Anaki D, Zion-Golumbic E, Bentin S. Electrophysiological neural mechanisms for detection, configural analysis and recognition of faces. Neuroimage. 2007;37(4):1407–16.CrossRefPubMed
40.
Itier RJ, Alain C, Sedore K, McIntosh AR. Early face processing specificity: It’s in the eyes! J Cogn Neurosci. 2007;19(11):1815–26.CrossRefPubMed
41.
S. J. Webb, R. Bernier, M. Paul, and G. Dawson, Further evidence for an abnormality in the temporal processing of faces in autism, 2003.
42.
Hileman CM, Henderson H, Mundy P, Newell L, Jaime M. Developmental and individual differences on the P1 and N170 ERP components in children with and without autism. Dev Neuropsychol. 2011;36(2):214–36.CrossRefPubMedPubMedCentral
43.
Güntekin B, Başar E. A review of brain oscillations in perception of faces and emotional pictures. Neuropsychologia. 2014;58(1):33–51.CrossRefPubMed
44.
Kaiser J, Lutzenberger W. Induced gamma-band activity and human brain function. Neuroscientist. 2003;9(6):475–84.CrossRefPubMed
45.
Wright B, et al. Gamma activation in young people with autism spectrum disorders and typically-developing controls when viewing emotions on faces. PLoS One. 2012;7:7.
46.
Herrmann CS, Fründ I, Lenz D. Human gamma-band activity: a review on cognitive and behavioral correlates and network models. Neurosci Biobehav Rev. 2010;34(7):981–92.CrossRefPubMed
47.
Rodriguez E, George N, Lachaux JP, Martinerie J, Renault B, Varela FJ. Perception’s shadow: long-distance synchronization of human brain activity. Nature. 1999;397(6718):430–3.CrossRefPubMed
48.
Grice SJ, et al. Disordered visual processing and oscillatory brain activity in autism and Williams syndrome. Neuroreport. 2001;12(12):2697–700.CrossRefPubMed
49.
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. 1994;24(5):659–85.CrossRefPubMed
50.
Lord C, et al. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000;30(3):205–23.CrossRefPubMed
51.
APA. Diagnostic and statistical manual of mental disorders, 4th text. Washington, D.C.: Author; 1994.
52.
Mooney CM. Age in the development of closure ability in children. Can J Psychol. 1957;11(4):219–26.CrossRefPubMed
53.
Chaumon M, Bishop DVM, Busch NA. A practical guide to the selection of independent components of the electroencephalogram for artifact correction. J Neurosci Methods. 2015;250:47–63.CrossRefPubMed
54.
Luck SJ. An Introduction to the Event-Related Potential Technique, Second Edition. Cambridge, MA: MIT Press; 2014.
55.
D’Hondt F, et al. Electrophysiological correlates of emotional face processing after mild traumatic brain injury in preschool children. Cogn Affect Behav Neurosci. 2017;17(1):124–42.CrossRefPubMed
56.
Tallon-Baudry C, Bertrand O, Delpuech C, Permier J. Oscillatory gamma-band (30-70 Hz) activity induced by a visual search task in humans. J Neurosci. 1997;17(2):722–34.CrossRefPubMed
57.
Castelhano J, Bernardino I, Rebola J, Rodriguez E, Castelo-Branco M. Oscillations or synchrony? Disruption of neural synchrony despite enhanced gamma oscillations in a model of disrupted perceptual coherence. J Cogn Neurosci. 2015;27(12):2416–26.CrossRefPubMed
58.
Wright B, et al. Gamma activation in young people with autism spectrum disorders and typically-developing controls when viewing emotions on faces. PLoS One. 2012;7(7):e41326.CrossRefPubMedPubMedCentral
59.
Wong TKW, Fung PCW, McAlonan GM, Chua SE. Spatiotemporal dipole source localization of face processing ERPs in adolescents: a preliminary study. Behav Brain Funct. 2009;5(1):16.CrossRefPubMedPubMedCentral
60.
Cecchini M, Aceto P, Altavilla D, Palumbo L, Lai C. The role of the eyes in processing an intact face and its scrambled image: a dense array ERP and low-resolution electromagnetic tomography (sLORETA) study. Soc Neurosci. 2013;8(4):314–25.CrossRefPubMed
61.
Sagiv N, Bentin S. Structural encoding of human and schematic faces: holistic and part-based processes. J Cogn Neurosci. 2001;13(7):937–51.CrossRefPubMed
62.
Herrmann CS, Munk MHJ, Engel AK. Cognitive functions of gamma-band activity: memory match and utilization. Trends Cogn Sci. 2004;8(8):347–55.CrossRefPubMed
63.
64.
Pellicano E, Burr D. When the world becomes ‘too real’: a Bayesian explanation of autistic perception. Trends Cogn Sci. 2012;16(10):504–10.CrossRefPubMed
65.
Stefanics G, Kremlacek J, Czigler I. Visual mismatch negativity: a predictive coding view. Front Hum Neurosci. 2014;8(September):1–19.
66.
Friston KJ, Lawson R, Frith CD. On hyperpriors and hypopriors: comment on Pellicano and Burr. Trends Cogn Sci. 2013;17(1):1.CrossRefPubMed
67.
Gao Z, Goldstein A, Harpaz Y, Hansel M, Zion-Golumbic E, Bentin S. A magnetoencephalographic study of face processing: M170, gamma-band oscillations and source localization. Hum Brain Mapp. 2013;34(8):1783–95.CrossRefPubMed
68.
Webb SJ, Neuhaus E, Faja S. Face perception and learning in autism spectrum disorders. Q J Exp Psychol. 2017;70(5):970–86.CrossRef
69.
Kessler K, Seymour RA, Rippon G. Brain oscillations and connectivity in autism spectrum disorders (ASD): new approaches to methodology, measurement and modelling. Neurosci Biobehav Rev. 2016;71:601–20.CrossRefPubMed
70.
David N, Schneider TR, Peiker I, Al-Jawahiri R, Engel AK, Milne E. Variability of cortical oscillation patterns: a possible endophenotype in autism spectrum disorders? Neurosci Biobehav Rev. 2016;71:590–600.CrossRefPubMed
Metadata
Title
Neurophysiological correlates of holistic face processing in adolescents with and without autism spectrum disorder
Authors
Sandra Naumann
Ulrike Senftleben
Megha Santhosh
James McPartland
Sara Jane Webb
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Neurodevelopmental Disorders / Issue 1/2018
Print ISSN: 1866-1947
Electronic ISSN: 1866-1955
DOI
https://doi.org/10.1186/s11689-018-9244-y

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