Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairment

The ability to rapidly discriminate successive auditory stimuli within tens-of-milliseconds is crucial for speech and language development, particularly in the first year of life. This skill, called Rapid Auditory Processing (RAP), is altered in infants at familial risk for language and learning imp...

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Main Authors: Chiara Cantiani, Silvia Ortiz-Mantilla, Valentina Riva, Caterina Piazza, Roberta Bettoni, Gabriella Musacchia, Massimo Molteni, Cecilia Marino, April A. Benasich
Format: Article
Language:English
Published: Elsevier 2019-01-01
Series:NeuroImage: Clinical
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158219301287
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author Chiara Cantiani
Silvia Ortiz-Mantilla
Valentina Riva
Caterina Piazza
Roberta Bettoni
Gabriella Musacchia
Massimo Molteni
Cecilia Marino
April A. Benasich
author_facet Chiara Cantiani
Silvia Ortiz-Mantilla
Valentina Riva
Caterina Piazza
Roberta Bettoni
Gabriella Musacchia
Massimo Molteni
Cecilia Marino
April A. Benasich
author_sort Chiara Cantiani
collection DOAJ
description The ability to rapidly discriminate successive auditory stimuli within tens-of-milliseconds is crucial for speech and language development, particularly in the first year of life. This skill, called Rapid Auditory Processing (RAP), is altered in infants at familial risk for language and learning impairment (LLI) and is a robust predictor of later language outcomes. In the present study, we investigate the neural substrates of RAP, i.e., the underlying neural oscillatory patterns, in a group of Italian 6-month-old infants at risk for LLI (FH+, n = 24), compared to control infants with no known family history of LLI (FH−, n = 32). Brain responses to rapid changes in fundamental frequency and duration were recorded via high-density electroencephalogram during a non-speech double oddball paradigm. Sources of event-related potential generators were localized to right and left auditory regions in both FH+ and FH− groups. Time-frequency analyses showed variations in both theta (Ɵ) and gamma (ɣ) ranges across groups. Our results showed that overall RAP stimuli elicited a more left-lateralized pattern of oscillations in FH− infants, whereas FH+ infants demonstrated a more right-lateralized pattern, in both the theta and gamma frequency bands. Interestingly, FH+ infants showed reduced early left gamma power (starting at 50 ms after stimulus onset) during deviant discrimination. Perturbed oscillatory dynamics may well constitute a candidate neural mechanism to explain group differences in RAP. Additional group differences in source location suggest that anatomical variations may underlie differences in oscillatory activity. Regarding the predictive value of early oscillatory measures, we found that the amplitude of the source response and the magnitude of oscillatory power and phase synchrony were predictive of expressive vocabulary at 20 months of age. These results further our understanding of the interplay among neural mechanisms that support typical and atypical rapid auditory processing in infancy. Keywords: Infants, Auditory processing, Language and learning impairment, EEG/ERP, Neural sources, Time-frequency analysis oscillations
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spelling doaj.art-bcd9ceae6d674f44a5f26d21fd7715372022-12-21T23:42:42ZengElsevierNeuroImage: Clinical2213-15822019-01-0122Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairmentChiara Cantiani0Silvia Ortiz-Mantilla1Valentina Riva2Caterina Piazza3Roberta Bettoni4Gabriella Musacchia5Massimo Molteni6Cecilia Marino7April A. Benasich8Child Psychopathology Unit, Scientific Institute, IRCCS E. Medea, Bosisio Parini, Lecco, Italy; Corresponding author at: Child Psychopathology Unit, Scientific Institute, IRCCS E. Medea, via don Luigi Monza, 20, 23842, Bosisio Parini, Lecco, Italy.Center for Molecular and Behavioral Neuroscience, Rutgers University-Newark, USAChild Psychopathology Unit, Scientific Institute, IRCCS E. Medea, Bosisio Parini, Lecco, ItalyBioengineering Lab, Scientific Institute IRCCS E. Medea, Bosisio Parini, Lecco, ItalyChild Psychopathology Unit, Scientific Institute, IRCCS E. Medea, Bosisio Parini, Lecco, Italy; Department of Psychology, University of Milano-Bicocca, Milano, ItalyDepartment of Audiology, University of the Pacific, USA; Department of Otolaryngology - Head and Neck Surgery, Stanford University, USAChild Psychopathology Unit, Scientific Institute, IRCCS E. Medea, Bosisio Parini, Lecco, ItalyCentre for Addiction and Mental Health (CAMH), University of Toronto, Toronto, CanadaCenter for Molecular and Behavioral Neuroscience, Rutgers University-Newark, USAThe ability to rapidly discriminate successive auditory stimuli within tens-of-milliseconds is crucial for speech and language development, particularly in the first year of life. This skill, called Rapid Auditory Processing (RAP), is altered in infants at familial risk for language and learning impairment (LLI) and is a robust predictor of later language outcomes. In the present study, we investigate the neural substrates of RAP, i.e., the underlying neural oscillatory patterns, in a group of Italian 6-month-old infants at risk for LLI (FH+, n = 24), compared to control infants with no known family history of LLI (FH−, n = 32). Brain responses to rapid changes in fundamental frequency and duration were recorded via high-density electroencephalogram during a non-speech double oddball paradigm. Sources of event-related potential generators were localized to right and left auditory regions in both FH+ and FH− groups. Time-frequency analyses showed variations in both theta (Ɵ) and gamma (ɣ) ranges across groups. Our results showed that overall RAP stimuli elicited a more left-lateralized pattern of oscillations in FH− infants, whereas FH+ infants demonstrated a more right-lateralized pattern, in both the theta and gamma frequency bands. Interestingly, FH+ infants showed reduced early left gamma power (starting at 50 ms after stimulus onset) during deviant discrimination. Perturbed oscillatory dynamics may well constitute a candidate neural mechanism to explain group differences in RAP. Additional group differences in source location suggest that anatomical variations may underlie differences in oscillatory activity. Regarding the predictive value of early oscillatory measures, we found that the amplitude of the source response and the magnitude of oscillatory power and phase synchrony were predictive of expressive vocabulary at 20 months of age. These results further our understanding of the interplay among neural mechanisms that support typical and atypical rapid auditory processing in infancy. Keywords: Infants, Auditory processing, Language and learning impairment, EEG/ERP, Neural sources, Time-frequency analysis oscillationshttp://www.sciencedirect.com/science/article/pii/S2213158219301287
spellingShingle Chiara Cantiani
Silvia Ortiz-Mantilla
Valentina Riva
Caterina Piazza
Roberta Bettoni
Gabriella Musacchia
Massimo Molteni
Cecilia Marino
April A. Benasich
Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairment
NeuroImage: Clinical
title Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairment
title_full Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairment
title_fullStr Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairment
title_full_unstemmed Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairment
title_short Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairment
title_sort reduced left lateralized pattern of event related eeg oscillations in infants at familial risk for language and learning impairment
url http://www.sciencedirect.com/science/article/pii/S2213158219301287
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