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

Author:

Symons Georgia F1,Clough Meaghan1,Mutimer Steven2,Major Brendan P1,O’Brien William T1,Costello Daniel2,McDonald Stuart J1,Chen Zhibin1,White Owen12,Mychasiuk Richelle1ORCID,Law Meng1,Wright David K1ORCID,O’Brien Terence J12,Fielding Joanne12,Kolbe Scott C1,Shultz Sandy R12ORCID

Affiliation:

1. Department of Neuroscience, Central Clinical School, Monash University, Melbourne, Australia

2. Department of Medicine, Royal Melbourne Hospital, University of Melbourne, Parkville, Australia

Abstract

Abstract 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.

Funder

Australian National Health and Medical Research Council (NHMRC) to S.R.S. R.M., T.J.O. and D.K.W

Publisher

Oxford University Press (OUP)

Subject

General Earth and Planetary Sciences,General Environmental Science

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