Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approach

Abstract Background Fragile X syndrome (FXS) is a neurodevelopmental genetic disorder causing cognitive and behavioural deficits. Repetition suppression (RS), a learning phenomenon in which stimulus repetitions result in diminished brain activity, has been found to be impaired in FXS. Alterations in...

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Main Authors: Inga Sophia Knoth, Tarek Lajnef, Simon Rigoulot, Karine Lacourse, Phetsamone Vannasing, Jacques L. Michaud, Sébastien Jacquemont, Philippe Major, Karim Jerbi, Sarah Lippé
Format: Article
Language:English
Published: BMC 2018-01-01
Series:Journal of Neurodevelopmental Disorders
Subjects:
EEG
Online Access:http://link.springer.com/article/10.1186/s11689-018-9223-3
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spelling doaj-0703e4d2c2c04da79cb91a66980c040b2020-11-24T23:17:58ZengBMCJournal of Neurodevelopmental Disorders1866-19471866-19552018-01-0110111310.1186/s11689-018-9223-3Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approachInga Sophia Knoth0Tarek Lajnef1Simon Rigoulot2Karine Lacourse3Phetsamone Vannasing4Jacques L. Michaud5Sébastien Jacquemont6Philippe Major7Karim Jerbi8Sarah Lippé9Neuroscience of Early Development (NED)Department of Psychology, Université de MontréalNeuroscience of Early Development (NED)Research Center of the CHU Sainte-Justine Mother and Child University Hospital CenterResearch Center of the CHU Sainte-Justine Mother and Child University Hospital CenterResearch Center of the CHU Sainte-Justine Mother and Child University Hospital CenterResearch Center of the CHU Sainte-Justine Mother and Child University Hospital CenterResearch Center of the CHU Sainte-Justine Mother and Child University Hospital CenterDepartment of Psychology, Université de MontréalNeuroscience of Early Development (NED)Abstract Background Fragile X syndrome (FXS) is a neurodevelopmental genetic disorder causing cognitive and behavioural deficits. Repetition suppression (RS), a learning phenomenon in which stimulus repetitions result in diminished brain activity, has been found to be impaired in FXS. Alterations in RS have been associated with behavioural problems in FXS; however, relations between RS and intellectual functioning have not yet been elucidated. Methods EEG was recorded in 14 FXS participants and 25 neurotypical controls during an auditory habituation paradigm using repeatedly presented pseudowords. Non-phased locked signal energy was compared across presentations and between groups using linear mixed models (LMMs) in order to investigate RS effects across repetitions and brain areas and a possible relation to non-verbal IQ (NVIQ) in FXS. In addition, we explored group differences according to NVIQ and we probed the feasibility of training a support vector machine to predict cognitive functioning levels across FXS participants based on single-trial RS features. Results LMM analyses showed that repetition effects differ between groups (FXS vs. controls) as well as with respect to NVIQ in FXS. When exploring group differences in RS patterns, we found that neurotypical controls revealed the expected pattern of RS between the first and second presentations of a pseudoword. More importantly, while FXS participants in the ≤ 42 NVIQ group showed no RS, the > 42 NVIQ group showed a delayed RS response after several presentations. Concordantly, single-trial estimates of repetition effects over the first four repetitions provided the highest decoding accuracies in the classification between the FXS participant groups. Conclusion Electrophysiological measures of repetition effects provide a non-invasive and unbiased measure of brain responses sensitive to cognitive functioning levels, which may be useful for clinical trials in FXS.http://link.springer.com/article/10.1186/s11689-018-9223-3Fragile X syndromeIntellectual disabilityEEGRepetition suppressionMachine learningHabituation
collection DOAJ
language English
format Article
sources DOAJ
author Inga Sophia Knoth
Tarek Lajnef
Simon Rigoulot
Karine Lacourse
Phetsamone Vannasing
Jacques L. Michaud
Sébastien Jacquemont
Philippe Major
Karim Jerbi
Sarah Lippé
spellingShingle Inga Sophia Knoth
Tarek Lajnef
Simon Rigoulot
Karine Lacourse
Phetsamone Vannasing
Jacques L. Michaud
Sébastien Jacquemont
Philippe Major
Karim Jerbi
Sarah Lippé
Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approach
Journal of Neurodevelopmental Disorders
Fragile X syndrome
Intellectual disability
EEG
Repetition suppression
Machine learning
Habituation
author_facet Inga Sophia Knoth
Tarek Lajnef
Simon Rigoulot
Karine Lacourse
Phetsamone Vannasing
Jacques L. Michaud
Sébastien Jacquemont
Philippe Major
Karim Jerbi
Sarah Lippé
author_sort Inga Sophia Knoth
title Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approach
title_short Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approach
title_full Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approach
title_fullStr Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approach
title_full_unstemmed Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approach
title_sort auditory repetition suppression alterations in relation to cognitive functioning in fragile x syndrome: a combined eeg and machine learning approach
publisher BMC
series Journal of Neurodevelopmental Disorders
issn 1866-1947
1866-1955
publishDate 2018-01-01
description Abstract Background Fragile X syndrome (FXS) is a neurodevelopmental genetic disorder causing cognitive and behavioural deficits. Repetition suppression (RS), a learning phenomenon in which stimulus repetitions result in diminished brain activity, has been found to be impaired in FXS. Alterations in RS have been associated with behavioural problems in FXS; however, relations between RS and intellectual functioning have not yet been elucidated. Methods EEG was recorded in 14 FXS participants and 25 neurotypical controls during an auditory habituation paradigm using repeatedly presented pseudowords. Non-phased locked signal energy was compared across presentations and between groups using linear mixed models (LMMs) in order to investigate RS effects across repetitions and brain areas and a possible relation to non-verbal IQ (NVIQ) in FXS. In addition, we explored group differences according to NVIQ and we probed the feasibility of training a support vector machine to predict cognitive functioning levels across FXS participants based on single-trial RS features. Results LMM analyses showed that repetition effects differ between groups (FXS vs. controls) as well as with respect to NVIQ in FXS. When exploring group differences in RS patterns, we found that neurotypical controls revealed the expected pattern of RS between the first and second presentations of a pseudoword. More importantly, while FXS participants in the ≤ 42 NVIQ group showed no RS, the > 42 NVIQ group showed a delayed RS response after several presentations. Concordantly, single-trial estimates of repetition effects over the first four repetitions provided the highest decoding accuracies in the classification between the FXS participant groups. Conclusion Electrophysiological measures of repetition effects provide a non-invasive and unbiased measure of brain responses sensitive to cognitive functioning levels, which may be useful for clinical trials in FXS.
topic Fragile X syndrome
Intellectual disability
EEG
Repetition suppression
Machine learning
Habituation
url http://link.springer.com/article/10.1186/s11689-018-9223-3
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