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

Chiara Cantiani; Silvia Ortiz-Mantilla; Valentina Riva; Caterina Piazza; Roberta Bettoni; Gabriella Musacchia; Massimo Molteni; Cecilia Marino; April A. Benasich

doi:10.1016/j.nicl.2019.101778

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

Chiara Cantiani, Silvia Ortiz-Mantilla, Valentina Riva, Caterina Piazza, Roberta Bettoni, Gabriella Musacchia, Massimo Molteni, Cecilia Marino, April A. Benasich

Rutgers, The State University

Research output: Contribution to journal › Article › peer-review

13 Scopus citations

Abstract

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.

Original language	American English
Article number	101778
Journal	NeuroImage: Clinical
Volume	22
DOIs	https://doi.org/10.1016/j.nicl.2019.101778
State	Published - Jan 1 2019

ASJC Scopus subject areas

Radiology Nuclear Medicine and imaging
Neurology
Clinical Neurology
Cognitive Neuroscience

Keywords

Auditory processing
EEG/ERP
Infants
Language and learning impairment
Neural sources
Time-frequency analysis oscillations

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10.1016/j.nicl.2019.101778

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

abstract = "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 = "Auditory processing, EEG/ERP, Infants, Language and learning impairment, Neural sources, Time-frequency analysis oscillations",

author = "Chiara Cantiani and Silvia Ortiz-Mantilla and Valentina Riva and Caterina Piazza and Roberta Bettoni and Gabriella Musacchia and Massimo Molteni and Cecilia Marino and Benasich, {April A.}",

note = "Funding Information: The authors wish to thank the nursing and clinical staff of the Department of Gynecology & Obstetrics of the Manzoni Hospital of Lecco and of the Hospital of Desio and Vimercate (branch of Carate Brianza). We are also grateful to Giulia Melesi and Giulia Mornati for their help in data collection and analyses. Finally, special thanks go to all infants and their parents participating in this study. This study was supported by the Italian Ministry of Health (Ricerca Corrente {"}2016, 2017, 2018, 2019{"} to dr {"}Chiara Cantiani{"}; Ricerca Finalizzata {"}NET-2013-02355263-2{"} and by the “ Fondazione Banca del Monte di Lombardia ” [Progetto Professionalit{\`a} Ivano Becchi]. Funding Information: The authors wish to thank the nursing and clinical staff of the Department of Gynecology & Obstetrics of the Manzoni Hospital of Lecco and of the Hospital of Desio and Vimercate (branch of Carate Brianza). We are also grateful to Giulia Melesi and Giulia Mornati for their help in data collection and analyses. Finally, special thanks go to all infants and their parents participating in this study. This study was supported by the Italian Ministry of Health (Ricerca Corrente “2016, 2017, 2018, 2019” to dr “Chiara Cantiani”; Ricerca Finalizzata “NET-2013-02355263-2” and by the “Fondazione Banca del Monte di Lombardia” [Progetto Professionalit{\`a} Ivano Becchi]. Publisher Copyright: {\textcopyright} 2019 The Authors",

year = "2019",

month = jan,

day = "1",

doi = "10.1016/j.nicl.2019.101778",

language = "American English",

volume = "22",

journal = "NeuroImage: Clinical",

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T1 - Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairment

AU - Cantiani, Chiara

AU - Ortiz-Mantilla, Silvia

AU - Riva, Valentina

AU - Piazza, Caterina

AU - Bettoni, Roberta

AU - Musacchia, Gabriella

AU - Molteni, Massimo

AU - Marino, Cecilia

AU - Benasich, April A.

N1 - Funding Information: The authors wish to thank the nursing and clinical staff of the Department of Gynecology & Obstetrics of the Manzoni Hospital of Lecco and of the Hospital of Desio and Vimercate (branch of Carate Brianza). We are also grateful to Giulia Melesi and Giulia Mornati for their help in data collection and analyses. Finally, special thanks go to all infants and their parents participating in this study. This study was supported by the Italian Ministry of Health (Ricerca Corrente "2016, 2017, 2018, 2019" to dr "Chiara Cantiani"; Ricerca Finalizzata "NET-2013-02355263-2" and by the “ Fondazione Banca del Monte di Lombardia ” [Progetto Professionalità Ivano Becchi]. Funding Information: The authors wish to thank the nursing and clinical staff of the Department of Gynecology & Obstetrics of the Manzoni Hospital of Lecco and of the Hospital of Desio and Vimercate (branch of Carate Brianza). We are also grateful to Giulia Melesi and Giulia Mornati for their help in data collection and analyses. Finally, special thanks go to all infants and their parents participating in this study. This study was supported by the Italian Ministry of Health (Ricerca Corrente “2016, 2017, 2018, 2019” to dr “Chiara Cantiani”; Ricerca Finalizzata “NET-2013-02355263-2” and by the “Fondazione Banca del Monte di Lombardia” [Progetto Professionalità Ivano Becchi]. Publisher Copyright: © 2019 The Authors

PY - 2019/1/1

Y1 - 2019/1/1

N2 - 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.

AB - 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.

KW - Auditory processing

KW - EEG/ERP

KW - Infants

KW - Language and learning impairment

KW - Neural sources

KW - Time-frequency analysis oscillations

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DO - 10.1016/j.nicl.2019.101778

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SN - 2213-1582

VL - 22

JO - NeuroImage: Clinical

JF - NeuroImage: Clinical

M1 - 101778

ER -

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

Abstract

ASJC Scopus subject areas

Keywords

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