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Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion

A history of concussion has been linked to long-term cognitive deficits; however, the neural underpinnings of these abnormalities are poorly understood. This study recruited 26 asymptomatic male Australian footballers with a remote history of concussion (i.e. at least six months since last concussio...

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Autores principales: Symons, Georgia F, Clough, Meaghan, Mutimer, Steven, Major, Brendan P, O’Brien, William T, Costello, Daniel, McDonald, Stuart J, Chen, Zhibin, White, Owen, Mychasiuk, Richelle, Law, Meng, Wright, David K, O’Brien, Terence J, Fielding, Joanne, Kolbe, Scott C, Shultz, Sandy R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8477916/
https://www.ncbi.nlm.nih.gov/pubmed/34595476
http://dx.doi.org/10.1093/braincomms/fcab213
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author Symons, Georgia F
Clough, Meaghan
Mutimer, Steven
Major, Brendan P
O’Brien, William T
Costello, Daniel
McDonald, Stuart J
Chen, Zhibin
White, Owen
Mychasiuk, Richelle
Law, Meng
Wright, David K
O’Brien, Terence J
Fielding, Joanne
Kolbe, Scott C
Shultz, Sandy R
author_facet Symons, Georgia F
Clough, Meaghan
Mutimer, Steven
Major, Brendan P
O’Brien, William T
Costello, Daniel
McDonald, Stuart J
Chen, Zhibin
White, Owen
Mychasiuk, Richelle
Law, Meng
Wright, David K
O’Brien, Terence J
Fielding, Joanne
Kolbe, Scott C
Shultz, Sandy R
author_sort Symons, Georgia F
collection PubMed
description A history of concussion has been linked to long-term cognitive deficits; however, the neural underpinnings of these abnormalities are poorly understood. This study recruited 26 asymptomatic male Australian footballers with a remote history of concussion (i.e. at least six months since last concussion), and 23 non-collision sport athlete controls with no history of concussion. Participants completed three ocular motor tasks (prosaccade, antisaccade and a cognitively complex switch task) to assess processing speed, inhibitory control and cognitive flexibility, respectively. Diffusion tensor imaging data were acquired using a 3 T MRI scanner, and analysed using tract-based spatial statistics, to investigate white matter abnormalities and how they relate to ocular motor performance. Australian footballers had significantly slower adjusted antisaccade latencies compared to controls (P = 0.035). A significant switch cost (i.e. switch trial error > repeat trial error) was also found on the switch task, with Australian footballers performing increased magnitude of errors on prosaccade switch trials relative to prosaccade repeat trials (P = 0.023). Diffusion tensor imaging analysis found decreased fractional anisotropy, a marker of white matter damage, in major white matter tracts (i.e. corpus callosum, corticospinal tract) in Australian footballers relative to controls. Notably, a larger prosaccade switch cost was significantly related to reduced fractional anisotropy in anterior white matter regions found to connect to the prefrontal cortex (i.e. a key cortical ocular motor centre involved in executive functioning and task switching). Taken together, Australian footballers with a history of concussion have ocular motor deficits indicative of poorer cognitive processing speed and cognitive flexibility, which are related to reduce white matter integrity in regions projecting to important cognitive ocular motor structures. These findings provide novel insights into the neural mechanisms that may underly chronic cognitive impairments in individuals with a history of concussion.
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spelling pubmed-84779162021-09-29 Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion Symons, Georgia F Clough, Meaghan Mutimer, Steven Major, Brendan P O’Brien, William T Costello, Daniel McDonald, Stuart J Chen, Zhibin White, Owen Mychasiuk, Richelle Law, Meng Wright, David K O’Brien, Terence J Fielding, Joanne Kolbe, Scott C Shultz, Sandy R Brain Commun Original Article A history of concussion has been linked to long-term cognitive deficits; however, the neural underpinnings of these abnormalities are poorly understood. This study recruited 26 asymptomatic male Australian footballers with a remote history of concussion (i.e. at least six months since last concussion), and 23 non-collision sport athlete controls with no history of concussion. Participants completed three ocular motor tasks (prosaccade, antisaccade and a cognitively complex switch task) to assess processing speed, inhibitory control and cognitive flexibility, respectively. Diffusion tensor imaging data were acquired using a 3 T MRI scanner, and analysed using tract-based spatial statistics, to investigate white matter abnormalities and how they relate to ocular motor performance. Australian footballers had significantly slower adjusted antisaccade latencies compared to controls (P = 0.035). A significant switch cost (i.e. switch trial error > repeat trial error) was also found on the switch task, with Australian footballers performing increased magnitude of errors on prosaccade switch trials relative to prosaccade repeat trials (P = 0.023). Diffusion tensor imaging analysis found decreased fractional anisotropy, a marker of white matter damage, in major white matter tracts (i.e. corpus callosum, corticospinal tract) in Australian footballers relative to controls. Notably, a larger prosaccade switch cost was significantly related to reduced fractional anisotropy in anterior white matter regions found to connect to the prefrontal cortex (i.e. a key cortical ocular motor centre involved in executive functioning and task switching). Taken together, Australian footballers with a history of concussion have ocular motor deficits indicative of poorer cognitive processing speed and cognitive flexibility, which are related to reduce white matter integrity in regions projecting to important cognitive ocular motor structures. These findings provide novel insights into the neural mechanisms that may underly chronic cognitive impairments in individuals with a history of concussion. Oxford University Press 2021-09-14 /pmc/articles/PMC8477916/ /pubmed/34595476 http://dx.doi.org/10.1093/braincomms/fcab213 Text en © The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Article
Symons, Georgia F
Clough, Meaghan
Mutimer, Steven
Major, Brendan P
O’Brien, William T
Costello, Daniel
McDonald, Stuart J
Chen, Zhibin
White, Owen
Mychasiuk, Richelle
Law, Meng
Wright, David K
O’Brien, Terence J
Fielding, Joanne
Kolbe, Scott C
Shultz, Sandy R
Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion
title Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion
title_full Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion
title_fullStr Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion
title_full_unstemmed Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion
title_short Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion
title_sort cognitive ocular motor deficits and white matter damage chronically after sports-related concussion
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8477916/
https://www.ncbi.nlm.nih.gov/pubmed/34595476
http://dx.doi.org/10.1093/braincomms/fcab213
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