Altered neural oscillations and connectivity in the beta band underlie detail-oriented visual processing in autism

Sensory and perceptual anomalies may have a major impact on basic cognitive and social skills in humans. Autism Spectrum Disorder (ASD) represents a special perspective to explore this relationship, being characterized by both these features. The present study employed electroencephalography (EEG) t...

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Main Authors: Luca Ronconi, Andrea Vitale, Alessandra Federici, Elisa Pini, Massimo Molteni, Luca Casartelli
Format: Article
Language:English
Published: Elsevier 2020-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158220303211
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spelling doaj-931de6da99614f658ca51a3dfd0195b42020-12-19T05:06:23ZengElsevierNeuroImage: Clinical2213-15822020-01-0128102484Altered neural oscillations and connectivity in the beta band underlie detail-oriented visual processing in autismLuca Ronconi0Andrea Vitale1Alessandra Federici2Elisa Pini3Massimo Molteni4Luca Casartelli5Faculty of Psychology, Vita-Salute San Raffaele University, Milan, Italy; IRCCS San Raffaele Scientific Institute, Milan, Italy; Theoretical and Cognitive Neuroscience Unit, Child Psychopathology Department, Scientific Institute IRCCS Eugenio Medea, Bosisio Parini, Italy; Corresponding authors at: School of Psychology, Vita-Salute San Raffaele University, Via Olgettina 58, 20132, Milan, Italy. IRCCS Eugenio Medea, Via Don Luigi Monza, 20, 23842, Bosisio Parini, Lecco, Italy (M. Molteni).Theoretical and Cognitive Neuroscience Unit, Child Psychopathology Department, Scientific Institute IRCCS Eugenio Medea, Bosisio Parini, ItalyTheoretical and Cognitive Neuroscience Unit, Child Psychopathology Department, Scientific Institute IRCCS Eugenio Medea, Bosisio Parini, Italy; IMT School of Advanced Studies Lucca, Lucca, ItalyTheoretical and Cognitive Neuroscience Unit, Child Psychopathology Department, Scientific Institute IRCCS Eugenio Medea, Bosisio Parini, Italy; Department of Psychology, University of Milano-Bicocca, Milano, ItalyChild Psychopathology Department, Scientific Institute IRCCS Eugenio Medea, Bosisio Parini, Italy; Corresponding authors at: School of Psychology, Vita-Salute San Raffaele University, Via Olgettina 58, 20132, Milan, Italy. IRCCS Eugenio Medea, Via Don Luigi Monza, 20, 23842, Bosisio Parini, Lecco, Italy (M. Molteni).Theoretical and Cognitive Neuroscience Unit, Child Psychopathology Department, Scientific Institute IRCCS Eugenio Medea, Bosisio Parini, ItalySensory and perceptual anomalies may have a major impact on basic cognitive and social skills in humans. Autism Spectrum Disorder (ASD) represents a special perspective to explore this relationship, being characterized by both these features. The present study employed electroencephalography (EEG) to test whether detail-oriented visual perception, a recognized hallmark of ASD, is associated with altered neural oscillations and functional connectivity in the beta frequency band, considering its role in feedback and top-down reentrant signalling in the typical population. Using a visual crowding task, where participants had to discriminate a peripheral target letter surrounded by flankers at different distances, we found that detail-oriented processing in children with ASD, as compared to typically developing peers, could be attributed to anomalous oscillatory activity in the beta band (15–30 Hz), while no differences emerged in the alpha band (8–12 Hz). Altered beta oscillatory response reflected in turn atypical functional connectivity between occipital areas, where the initial stimulus analysis is accomplished, and infero-temporal regions, where objects identity is extracted. Such atypical beta connectivity predicted both ASD symptomatology and their detail-oriented processing. Overall, these results might be explained by an altered feedback connectivity within the visual system, with potential cascade effects in visual scene parsing and higher order functions.http://www.sciencedirect.com/science/article/pii/S2213158220303211VisionBeta oscillationsLocal perceptionEEG connectivityHyperconnectivityVisual system
collection DOAJ
language English
format Article
sources DOAJ
author Luca Ronconi
Andrea Vitale
Alessandra Federici
Elisa Pini
Massimo Molteni
Luca Casartelli
spellingShingle Luca Ronconi
Andrea Vitale
Alessandra Federici
Elisa Pini
Massimo Molteni
Luca Casartelli
Altered neural oscillations and connectivity in the beta band underlie detail-oriented visual processing in autism
NeuroImage: Clinical
Vision
Beta oscillations
Local perception
EEG connectivity
Hyperconnectivity
Visual system
author_facet Luca Ronconi
Andrea Vitale
Alessandra Federici
Elisa Pini
Massimo Molteni
Luca Casartelli
author_sort Luca Ronconi
title Altered neural oscillations and connectivity in the beta band underlie detail-oriented visual processing in autism
title_short Altered neural oscillations and connectivity in the beta band underlie detail-oriented visual processing in autism
title_full Altered neural oscillations and connectivity in the beta band underlie detail-oriented visual processing in autism
title_fullStr Altered neural oscillations and connectivity in the beta band underlie detail-oriented visual processing in autism
title_full_unstemmed Altered neural oscillations and connectivity in the beta band underlie detail-oriented visual processing in autism
title_sort altered neural oscillations and connectivity in the beta band underlie detail-oriented visual processing in autism
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2020-01-01
description Sensory and perceptual anomalies may have a major impact on basic cognitive and social skills in humans. Autism Spectrum Disorder (ASD) represents a special perspective to explore this relationship, being characterized by both these features. The present study employed electroencephalography (EEG) to test whether detail-oriented visual perception, a recognized hallmark of ASD, is associated with altered neural oscillations and functional connectivity in the beta frequency band, considering its role in feedback and top-down reentrant signalling in the typical population. Using a visual crowding task, where participants had to discriminate a peripheral target letter surrounded by flankers at different distances, we found that detail-oriented processing in children with ASD, as compared to typically developing peers, could be attributed to anomalous oscillatory activity in the beta band (15–30 Hz), while no differences emerged in the alpha band (8–12 Hz). Altered beta oscillatory response reflected in turn atypical functional connectivity between occipital areas, where the initial stimulus analysis is accomplished, and infero-temporal regions, where objects identity is extracted. Such atypical beta connectivity predicted both ASD symptomatology and their detail-oriented processing. Overall, these results might be explained by an altered feedback connectivity within the visual system, with potential cascade effects in visual scene parsing and higher order functions.
topic Vision
Beta oscillations
Local perception
EEG connectivity
Hyperconnectivity
Visual system
url http://www.sciencedirect.com/science/article/pii/S2213158220303211
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