A precision neuroscience approach to estimating reliability of neural responses during emotion processing: Implications for task-fMRI

Recent work demonstrating low test-retest reliability of neural activation during fMRI tasks raises questions about the utility of task-based fMRI for the study of individual variation in brain function. Two possible sources of the instability in task-based BOLD signal over time are noise or measure...

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Main Authors: John C. Flournoy, Nessa V. Bryce, Meg J. Dennison, Alexandra M. Rodman, Elizabeth A. McNeilly, Lucy A. Lurie, Debbie Bitran, Azure Reid-Russell, Constanza M. Vidal Bustamante, Tara Madhyastha, Katie A. McLaughlin
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811923006535
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author John C. Flournoy
Nessa V. Bryce
Meg J. Dennison
Alexandra M. Rodman
Elizabeth A. McNeilly
Lucy A. Lurie
Debbie Bitran
Azure Reid-Russell
Constanza M. Vidal Bustamante
Tara Madhyastha
Katie A. McLaughlin
author_facet John C. Flournoy
Nessa V. Bryce
Meg J. Dennison
Alexandra M. Rodman
Elizabeth A. McNeilly
Lucy A. Lurie
Debbie Bitran
Azure Reid-Russell
Constanza M. Vidal Bustamante
Tara Madhyastha
Katie A. McLaughlin
author_sort John C. Flournoy
collection DOAJ
description Recent work demonstrating low test-retest reliability of neural activation during fMRI tasks raises questions about the utility of task-based fMRI for the study of individual variation in brain function. Two possible sources of the instability in task-based BOLD signal over time are noise or measurement error in the instrument, and meaningful variation across time within-individuals in the construct itself—brain activation elicited during fMRI tasks. Examining the contribution of these two sources of test-retest unreliability in task-evoked brain activity has far-reaching implications for cognitive neuroscience. If test-retest reliability largely reflects measurement error, it suggests that task-based fMRI has little utility in the study of either inter- or intra-individual differences. On the other hand, if task-evoked BOLD signal varies meaningfully over time, it would suggest that this tool may yet be well suited to studying intraindividual variation. We parse these sources of variance in BOLD signal in response to emotional cues over time and within-individuals in a longitudinal sample with 10 monthly fMRI scans. Test-retest reliability was low, reflecting a lack of stability in between-person differences across scans. In contrast, within-person, within-session internal consistency of the BOLD signal was higher, and within-person fluctuations across sessions explained almost half the variance in voxel-level neural responses. Additionally, monthly fluctuations in neural response to emotional cues were associated with intraindividual variation in mood, sleep, and exposure to stressors. Rather than reflecting trait-like differences across people, neural responses to emotional cues may be more reflective of intraindividual variation over time. These patterns suggest that task-based fMRI may be able to contribute to the study of individual variation in brain function if more attention is given to within-individual variation approaches, psychometrics—beginning with improving reliability beyond the modest estimates observed here, and the validity of task fMRI beyond the suggestive associations reported here.
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spelling doaj.art-d35de135d83241de92658690555963422024-01-10T04:35:18ZengElsevierNeuroImage1095-95722024-01-01285120503A precision neuroscience approach to estimating reliability of neural responses during emotion processing: Implications for task-fMRIJohn C. Flournoy0Nessa V. Bryce1Meg J. Dennison2Alexandra M. Rodman3Elizabeth A. McNeilly4Lucy A. Lurie5Debbie Bitran6Azure Reid-Russell7Constanza M. Vidal Bustamante8Tara Madhyastha9Katie A. McLaughlin10Department of Psychology, Harvard University; Corresponding author at: Department of Psychology, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, USA.Department of Psychology, Harvard UniversityPhoenix Australia—Centre for Posttraumatic Mental Health, Department of Psychiatry, The University of Melbourne, Melbourne, VIC, AustraliaDepartment of Psychology, Harvard UniversityDepartment of Psychology, University of OregonDepartment of Psychology and Neuroscience, University of North Carolina at Chapel HillDepartment of Psychology, Harvard University; Phoenix Australia—Centre for Posttraumatic Mental Health, Department of Psychiatry, The University of Melbourne, Melbourne, VIC, Australia; Department of Psychology, University of Oregon; Department of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Rescale; Department of Psychology, University of Pittsburgh; Integrated Brain Imaging Center, University of WashingtonDepartment of Psychology, Harvard UniversityDepartment of Psychology, Harvard UniversityRescaleDepartment of Psychology, Harvard UniversityRecent work demonstrating low test-retest reliability of neural activation during fMRI tasks raises questions about the utility of task-based fMRI for the study of individual variation in brain function. Two possible sources of the instability in task-based BOLD signal over time are noise or measurement error in the instrument, and meaningful variation across time within-individuals in the construct itself—brain activation elicited during fMRI tasks. Examining the contribution of these two sources of test-retest unreliability in task-evoked brain activity has far-reaching implications for cognitive neuroscience. If test-retest reliability largely reflects measurement error, it suggests that task-based fMRI has little utility in the study of either inter- or intra-individual differences. On the other hand, if task-evoked BOLD signal varies meaningfully over time, it would suggest that this tool may yet be well suited to studying intraindividual variation. We parse these sources of variance in BOLD signal in response to emotional cues over time and within-individuals in a longitudinal sample with 10 monthly fMRI scans. Test-retest reliability was low, reflecting a lack of stability in between-person differences across scans. In contrast, within-person, within-session internal consistency of the BOLD signal was higher, and within-person fluctuations across sessions explained almost half the variance in voxel-level neural responses. Additionally, monthly fluctuations in neural response to emotional cues were associated with intraindividual variation in mood, sleep, and exposure to stressors. Rather than reflecting trait-like differences across people, neural responses to emotional cues may be more reflective of intraindividual variation over time. These patterns suggest that task-based fMRI may be able to contribute to the study of individual variation in brain function if more attention is given to within-individual variation approaches, psychometrics—beginning with improving reliability beyond the modest estimates observed here, and the validity of task fMRI beyond the suggestive associations reported here.http://www.sciencedirect.com/science/article/pii/S1053811923006535fMRIReliabilityNeuroimagingLongitudinalIndividual differencesTranslational neuroscience
spellingShingle John C. Flournoy
Nessa V. Bryce
Meg J. Dennison
Alexandra M. Rodman
Elizabeth A. McNeilly
Lucy A. Lurie
Debbie Bitran
Azure Reid-Russell
Constanza M. Vidal Bustamante
Tara Madhyastha
Katie A. McLaughlin
A precision neuroscience approach to estimating reliability of neural responses during emotion processing: Implications for task-fMRI
NeuroImage
fMRI
Reliability
Neuroimaging
Longitudinal
Individual differences
Translational neuroscience
title A precision neuroscience approach to estimating reliability of neural responses during emotion processing: Implications for task-fMRI
title_full A precision neuroscience approach to estimating reliability of neural responses during emotion processing: Implications for task-fMRI
title_fullStr A precision neuroscience approach to estimating reliability of neural responses during emotion processing: Implications for task-fMRI
title_full_unstemmed A precision neuroscience approach to estimating reliability of neural responses during emotion processing: Implications for task-fMRI
title_short A precision neuroscience approach to estimating reliability of neural responses during emotion processing: Implications for task-fMRI
title_sort precision neuroscience approach to estimating reliability of neural responses during emotion processing implications for task fmri
topic fMRI
Reliability
Neuroimaging
Longitudinal
Individual differences
Translational neuroscience
url http://www.sciencedirect.com/science/article/pii/S1053811923006535
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