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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Veröffentlicht in:	NeuroImage (Orlando, Fla.) Jg. 282; S. 120390
Hauptverfasser:	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
Sprache:	Englisch
Veröffentlicht:	United States Elsevier Inc 15.11.2023 Elsevier Limited Elsevier
Schlagworte:	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 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
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	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. •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.
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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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/37751811$$D View this record in MEDLINE/PubMed
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CitedBy_id	crossref_primary_10_1016_j_isci_2025_112922 crossref_primary_10_1073_pnas_2511101122 crossref_primary_10_1093_scan_nsae086 crossref_primary_10_1093_cercor_bhae100 crossref_primary_10_1016_j_neuroimage_2025_121255 crossref_primary_10_1016_j_neuroimage_2024_120890 crossref_primary_10_1073_pnas_2401317121 crossref_primary_10_3390_bs15091243 crossref_primary_10_1111_psyp_70005 crossref_primary_10_1016_j_dcn_2024_101362 crossref_primary_10_1162_IMAG_a_101 crossref_primary_10_1016_j_neuropsychologia_2023_108763 crossref_primary_10_1109_TBME_2024_3423703
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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
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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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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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