Ethan M. McCormick
Poorer White Matter Microstructure Predicts Slower and More Variable Reaction Time Performance: Evidence for a Neural Noise Hypothesis in a Large Lifespan Cohort
McCormick, Ethan M.; Kievit, Rogier A.; Tyler, Lorraine K.; Brayne, Carol; Bullmore, Edward T.; Calder, Andrew C.; Cusack, Rhodri; Dalgleish, Tim; Duncan, John; Henson, Richard N.; Matthews, Fiona E.; Marslen-Wilson, William D.; Rowe, James B.; Shafto, Meredith A.; Associates, Research; Campbell, Karen; Cheung, Teresa; Davis, Simon; Geerligs, Linda; McCarrey, Anna; Mustafa, Abdur; Price, Darren; Samu, David; Taylor, Jason R.; Treder, Matthias; Tsvetanov, Kamen A.; van Belle, Janna; Williams, Nitin; Bates, Lauren; Emery, Tina; Erzinçlioglu, Sharon; Gadie, Andrew; Gerbase, Sofia; Georgieva, Stanimira; Hanley, Claire; Parkin, Beth; Troy, David; Auer, Tibor; Correia, Marta; Gao, Lu; Green, Emma; Henriques, Rafael; Allen, Jodie; Amery, Gillian; Amunts, Liana; Barcroft, Anne; Castle, Amanda; Dias, Cheryl; Dowrick, Jonathan; Fair, Melissa; Fisher, Hayley; Goulding, Anna; Grewal, Adarsh; Hale, Geoff; Hilton, Andrew; Johnson, Frances; Johnston, Patricia; Kavanagh-Williamson, Thea; Kwasniewska,...
Authors
Rogier A. Kievit
Lorraine K. Tyler
Carol Brayne
Edward T. Bullmore
Andrew C. Calder
Rhodri Cusack
Tim Dalgleish
John Duncan
Richard N. Henson
Professor Fiona Matthews F.Matthews@hull.ac.uk
Pro-Vice-Chancellor Research and Enterprise
William D. Marslen-Wilson
James B. Rowe
Meredith A. Shafto
Research Associates
Karen Campbell
Teresa Cheung
Simon Davis
Linda Geerligs
Anna McCarrey
Abdur Mustafa
Darren Price
David Samu
Jason R. Taylor
Matthias Treder
Kamen A. Tsvetanov
Janna van Belle
Nitin Williams
Lauren Bates
Tina Emery
Sharon Erzinçlioglu
Andrew Gadie
Sofia Gerbase
Stanimira Georgieva
Claire Hanley
Beth Parkin
David Troy
Tibor Auer
Marta Correia
Lu Gao
Emma Green
Rafael Henriques
Jodie Allen
Gillian Amery
Liana Amunts
Anne Barcroft
Amanda Castle
Cheryl Dias
Jonathan Dowrick
Melissa Fair
Hayley Fisher
Anna Goulding
Adarsh Grewal
Geoff Hale
Andrew Hilton
Frances Johnson
Patricia Johnston
Thea Kavanagh-Williamson
Magdalena Kwasniewska
Alison McMinn
Kim Norman
Jessica Penrose
Fiona Roby
Diane Rowland
John Sargeant
Maggie Squire
Beth Stevens
Aldabra Stoddart
Cheryl Stone
Tracy Thompson
Ozlem Yazlik
Dan Barnes
Marie Dixon
Jaya Hillman
Joanne Mitchell
Laura Villis
Ethan Knights
Abstract
Most prior research has focused on characterizing averages in cognition, brain characteristics, or behavior, and attempting to predict differences in these averages among individuals. However, this overwhelming focus on mean levels may leave us with an incomplete picture of what drives individual differences in behavioral phenotypes by ignoring the variability of behavior around an individual's mean. In particular, enhanced white matter (WM) structural microstructure has been hypothesized to support consistent behavioral performance by decreasing Gaussian noise in signal transfer. Conversely, lower indices of WM microstructure are associated with greater within-subject variance in the ability to deploy performance-related resources, especially in clinical populations. We tested a mechanistic account of the “neural noise” hypothesis in a large adult lifespan cohort (Cambridge Centre for Ageing and Neuroscience) with over 2500 adults (ages 18-102; 1508 female; 1173 male; 2681 behavioral sessions; 708 MRI scans) using WM fractional anisotropy to predict mean levels and variability in reaction time performance on a simple behavioral task using a dynamic structural equation model. By modeling robust and reliable individual differences in within-person variability, we found support for a neural noise hypothesis (Kail, 1997), with lower fractional anisotropy predicted individual differences in separable components of behavioral performance estimated using dynamic structural equation model, including slower mean responses and increased variability. These effects remained when including age, suggesting consistent effects of WM microstructure across the adult lifespan unique from concurrent effects of aging. Crucially, we show that variability can be reliably separated from mean performance using advanced modeling tools, enabling tests of distinct hypotheses for each component of performance.
Citation
McCormick, E. M., Kievit, R. A., Tyler, L. K., Brayne, C., Bullmore, E. T., Calder, A. C., Cusack, R., Dalgleish, T., Duncan, J., Henson, R. N., Matthews, F. E., Marslen-Wilson, W. D., Rowe, J. B., Shafto, M. A., Associates, R., Campbell, K., Cheung, T., Davis, S., Geerligs, L., McCarrey, A., …Knights, E. (2023). Poorer White Matter Microstructure Predicts Slower and More Variable Reaction Time Performance: Evidence for a Neural Noise Hypothesis in a Large Lifespan Cohort. Journal of Neuroscience, 43(19), 3557-3566. https://doi.org/10.1523/JNEUROSCI.1042-22.2023
Journal Article Type | Article |
---|---|
Acceptance Date | Feb 15, 2023 |
Online Publication Date | Apr 7, 2023 |
Publication Date | May 10, 2023 |
Deposit Date | Mar 30, 2024 |
Publicly Available Date | Apr 2, 2024 |
Journal | Journal of Neuroscience |
Print ISSN | 0270-6474 |
Electronic ISSN | 1529-2401 |
Publisher | Society for Neuroscience |
Peer Reviewed | Peer Reviewed |
Volume | 43 |
Issue | 19 |
Pages | 3557-3566 |
DOI | https://doi.org/10.1523/JNEUROSCI.1042-22.2023 |
Keywords | Aging; Dynamic structural equation modeling; Lifespan; Reaction time; White matter |
Public URL | https://hull-repository.worktribe.com/output/4496290 |
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Copyright Statement
Copyright © 2023 McCormick et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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