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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

Ethan M. McCormick

Rogier A. Kievit

Lorraine K. Tyler

Carol Brayne

Edward T. Bullmore

Andrew C. Calder

Rhodri Cusack

Tim Dalgleish

John Duncan

Richard N. Henson

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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Publisher Licence URL
http://creativecommons.org/licenses/by/4.0

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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