Inter-subject correlation during long narratives reveals widespread neural correlates of reading ability

•75 adolescents read and heard time-locked narratives during an fMRI scan.•Inter-subject correlation (ISC) was used to analyze reading ability's impact.•ISC was more sensitive to individual differences in reading ability than GLMs.•Reading ability affects brain activity in more regions than pre...

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Published in:NeuroImage (Orlando, Fla.) Vol. 282; p. 120390
Main Authors: Jangraw, David C., Finn, Emily S., Bandettini, Peter A., Landi, Nicole, Sun, Haorui, Hoeft, Fumiko, Chen, Gang, Pugh, Kenneth R., Molfese, Peter J.
Format: Journal Article
Language:English
Published: United States Elsevier Inc 15.11.2023
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ISSN:1053-8119, 1095-9572, 1095-9572
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Abstract •75 adolescents read and heard time-locked narratives during an fMRI scan.•Inter-subject correlation (ISC) was used to analyze reading ability's impact.•ISC was more sensitive to individual differences in reading ability than GLMs.•Reading ability affects brain activity in more regions than previously thought.•Worse readers had more idiosyncratic responses than better readers across the brain. Recent work using fMRI inter-subject correlation analysis has provided new information about the brain's response to video and audio narratives, particularly in frontal regions not typically activated by single words. This approach is very well suited to the study of reading, where narrative is central to natural experience. But since past reading paradigms have primarily presented single words or phrases, the influence of narrative on semantic processing in the brain – and how that influence might change with reading ability – remains largely unexplored. In this study, we presented coherent stories to adolescents and young adults with a wide range of reading abilities. The stories were presented in alternating visual and auditory blocks. We used a dimensional inter-subject correlation analysis to identify regions in which better and worse readers had varying levels of consistency with other readers. This analysis identified a widespread set of brain regions in which activity timecourses were more similar among better readers than among worse readers. These differences were not detected with standard block activation analyses. Worse readers had higher correlation with better readers than with other worse readers, suggesting that the worse readers had “idiosyncratic” responses rather than using a single compensatory mechanism. Close inspection confirmed that these differences were not explained by differences in IQ or motion. These results suggest an expansion of the current view of where and how reading ability is reflected in the brain, and in doing so, they establish inter-subject correlation as a sensitive tool for future studies of reading disorders.
AbstractList •75 adolescents read and heard time-locked narratives during an fMRI scan.•Inter-subject correlation (ISC) was used to analyze reading ability's impact.•ISC was more sensitive to individual differences in reading ability than GLMs.•Reading ability affects brain activity in more regions than previously thought.•Worse readers had more idiosyncratic responses than better readers across the brain. Recent work using fMRI inter-subject correlation analysis has provided new information about the brain's response to video and audio narratives, particularly in frontal regions not typically activated by single words. This approach is very well suited to the study of reading, where narrative is central to natural experience. But since past reading paradigms have primarily presented single words or phrases, the influence of narrative on semantic processing in the brain – and how that influence might change with reading ability – remains largely unexplored. In this study, we presented coherent stories to adolescents and young adults with a wide range of reading abilities. The stories were presented in alternating visual and auditory blocks. We used a dimensional inter-subject correlation analysis to identify regions in which better and worse readers had varying levels of consistency with other readers. This analysis identified a widespread set of brain regions in which activity timecourses were more similar among better readers than among worse readers. These differences were not detected with standard block activation analyses. Worse readers had higher correlation with better readers than with other worse readers, suggesting that the worse readers had “idiosyncratic” responses rather than using a single compensatory mechanism. Close inspection confirmed that these differences were not explained by differences in IQ or motion. These results suggest an expansion of the current view of where and how reading ability is reflected in the brain, and in doing so, they establish inter-subject correlation as a sensitive tool for future studies of reading disorders.
Recent work using fMRI inter-subject correlation analysis has provided new information about the brain's response to video and audio narratives, particularly in frontal regions not typically activated by single words. This approach is very well suited to the study of reading, where narrative is central to natural experience. But since past reading paradigms have primarily presented single words or phrases, the influence of narrative on semantic processing in the brain - and how that influence might change with reading ability - remains largely unexplored. In this study, we presented coherent stories to adolescents and young adults with a wide range of reading abilities. The stories were presented in alternating visual and auditory blocks. We used a dimensional inter-subject correlation analysis to identify regions in which better and worse readers had varying levels of consistency with other readers. This analysis identified a widespread set of brain regions in which activity timecourses were more similar among better readers than among worse readers. These differences were not detected with standard block activation analyses. Worse readers had higher correlation with better readers than with other worse readers, suggesting that the worse readers had "idiosyncratic" responses rather than using a single compensatory mechanism. Close inspection confirmed that these differences were not explained by differences in IQ or motion. These results suggest an expansion of the current view of where and how reading ability is reflected in the brain, and in doing so, they establish inter-subject correlation as a sensitive tool for future studies of reading disorders.
Recent work using fMRI inter-subject correlation analysis has provided new information about the brain's response to video and audio narratives, particularly in frontal regions not typically activated by single words. This approach is very well suited to the study of reading, where narrative is central to natural experience. But since past reading paradigms have primarily presented single words or phrases, the influence of narrative on semantic processing in the brain - and how that influence might change with reading ability - remains largely unexplored. In this study, we presented coherent stories to adolescents and young adults with a wide range of reading abilities. The stories were presented in alternating visual and auditory blocks. We used a dimensional inter-subject correlation analysis to identify regions in which better and worse readers had varying levels of consistency with other readers. This analysis identified a widespread set of brain regions in which activity timecourses were more similar among better readers than among worse readers. These differences were not detected with standard block activation analyses. Worse readers had higher correlation with better readers than with other worse readers, suggesting that the worse readers had "idiosyncratic" responses rather than using a single compensatory mechanism. Close inspection confirmed that these differences were not explained by differences in IQ or motion. These results suggest an expansion of the current view of where and how reading ability is reflected in the brain, and in doing so, they establish inter-subject correlation as a sensitive tool for future studies of reading disorders.Recent work using fMRI inter-subject correlation analysis has provided new information about the brain's response to video and audio narratives, particularly in frontal regions not typically activated by single words. This approach is very well suited to the study of reading, where narrative is central to natural experience. But since past reading paradigms have primarily presented single words or phrases, the influence of narrative on semantic processing in the brain - and how that influence might change with reading ability - remains largely unexplored. In this study, we presented coherent stories to adolescents and young adults with a wide range of reading abilities. The stories were presented in alternating visual and auditory blocks. We used a dimensional inter-subject correlation analysis to identify regions in which better and worse readers had varying levels of consistency with other readers. This analysis identified a widespread set of brain regions in which activity timecourses were more similar among better readers than among worse readers. These differences were not detected with standard block activation analyses. Worse readers had higher correlation with better readers than with other worse readers, suggesting that the worse readers had "idiosyncratic" responses rather than using a single compensatory mechanism. Close inspection confirmed that these differences were not explained by differences in IQ or motion. These results suggest an expansion of the current view of where and how reading ability is reflected in the brain, and in doing so, they establish inter-subject correlation as a sensitive tool for future studies of reading disorders.
ArticleNumber 120390
Author Sun, Haorui
Molfese, Peter J.
Landi, Nicole
Jangraw, David C.
Chen, Gang
Pugh, Kenneth R.
Bandettini, Peter A.
Finn, Emily S.
Hoeft, Fumiko
AuthorAffiliation 4. Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH
1. Section on Functional Imaging Methods, NIMH, Bethesda, MD
2. Emotion and Development Branch, NIMH, Bethesda, MD
8. Statistical Computing Core, NIMH, Bethesda, MD
6. Haskins Laboratories, New Haven, CT
5. Center for Multimodal Neuroimaging, NIMH, Bethesda, MD
3. Department of Electrical and Biomedical Engineering, University of Vermont, Burlington, VT
7. Department of Psychological Sciences, University of Connecticut, Hartford, CT
9. Department of Pediatrics, Yale University School of Medicine, New Haven, CT
AuthorAffiliation_xml – name: 5. Center for Multimodal Neuroimaging, NIMH, Bethesda, MD
– name: 8. Statistical Computing Core, NIMH, Bethesda, MD
– name: 2. Emotion and Development Branch, NIMH, Bethesda, MD
– name: 3. Department of Electrical and Biomedical Engineering, University of Vermont, Burlington, VT
– name: 9. Department of Pediatrics, Yale University School of Medicine, New Haven, CT
– name: 4. Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH
– name: 1. Section on Functional Imaging Methods, NIMH, Bethesda, MD
– name: 7. Department of Psychological Sciences, University of Connecticut, Hartford, CT
– name: 6. Haskins Laboratories, New Haven, CT
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  orcidid: 0000-0002-3045-9408
  surname: Molfese
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37751811$$D View this record in MEDLINE/PubMed
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Keywords IPL
MidFG
STG
WASI
GLM
SPL
LingG
VWFA
Narrative
Naturalistic
BOLD
Cun
Oc-T
pCun
Precun
AG
SMA
IQ
TOWRE
SMG
ROI
PCA
fMRI
FWHM
PreCG
NN
WJ3
IS-RSA
CalG
CerVer
IFG
AnnaK
FDR
IFG-pOper-pTri
ISC
IOG
ACC
DLPFC
Fus
LME
FEF
MidCC
SOG
MidOG
Reading
MidTG
TMP
TP
Inter-subject correlation
TR
EPI
Language English
License This is an open access article under the CC BY license.
Copyright © 2023. Published by Elsevier Inc.
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Snippet •75 adolescents read and heard time-locked narratives during an fMRI scan.•Inter-subject correlation (ISC) was used to analyze reading ability's impact.•ISC...
Recent work using fMRI inter-subject correlation analysis has provided new information about the brain's response to video and audio narratives, particularly...
Recent work using fMRI inter-subject correlation analysis has provided new information about the brain’s response to video and audio narratives, particularly...
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StartPage 120390
SubjectTerms Adolescent
Brain - diagnostic imaging
Brain - physiology
Brain Mapping
Brain research
Cognition
Correlation analysis
Dyslexia
Efficiency
fMRI
Functional magnetic resonance imaging
Humans
Hypotheses
Information processing
Inter-subject correlation
Language
Magnetic Resonance Imaging
Medical imaging
Narrative
Narratives
Naturalism
Naturalistic
Neuroimaging
Reading
Reading disabilities
Semantics
Sensory integration
Teenagers
Young Adult
Young adults
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Title Inter-subject correlation during long narratives reveals widespread neural correlates of reading ability
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