Abstract
BackgroundImpaired eye movements in multiple sclerosis (MS) are common and could represent a non-invasive and accurate measure of (dys)functioning of interconnected areas within the complex brain network. The aim of this study was to test whether altered saccadic eye movements are related to changes in functional connectivity (FC) in patients with MS. MethodsCross-sectional eye movement (pro-saccades and anti-saccades) and magnetoencephalography (MEG) data from the Amsterdam MS cohort were included from 176 MS patients and 33 healthy controls. FC was calculated between all regions of the Brainnetome atlas in six conventional frequency bands. Cognitive function and disability were evaluated by previously validated measures. The relationships between saccadic parameters and both FC and clinical scores in MS patients were analysed using multivariate linear regression models. ResultsIn MS pro- and anti-saccades were abnormal compared to healthy controls A relationship of saccadic eye movements was found with FC of the oculomotor network, which was stronger for regional than global FC. In general, abnormal eye movements were related to higher delta and theta FC but lower beta FC. Strongest associations were found for pro-saccadic latency and FC of the precuneus (beta band β = -0.23, p = .006), peak velocity and FC of the parietal eye field (theta band β = -0.25, p = .005) and gain and FC of the inferior frontal eye field (theta band β = -0.25, p = .003). Pro-saccadic latency was also strongly associated with disability scores and cognitive dysfunction. ConclusionsImpaired saccadic eye movements were related to functional connectivity of the oculomotor network and clinical performance in MS. This study also showed that, in addition to global network connectivity, studying regional changes in MEG studies could yield stronger correlations.
Highlights
The shift in focus from studying focal pathology to functional brain networks has increased our understanding of the etiology of clinical dysfunction, which is especially relevant in multiple sclerosis (MS). (Mollison et al, 2017; Schoonheim et al, 2014; Schoonheim et al, 2015) Functional brain network inefficiency result ing from accumulating structural damage varies between individuals, Abbreviations: MS, multiple sclerosis; FC, functional connectivity; MEG, magnetoencephalography; INO, internuclear ophthalmoplegia; EDSS, Expanded Disability Status Scale; peak velocity by the saccadic amplitude (Pv/Am), peak velocity divided by amplitude; BNA, Brainnetome Network Atlas; AECc, corrected Amplitude Envelope Correlation
This study showed that altered saccadic parameters in MS are related to FC of the oculomotor network
Saccadic parameters were related to clinical outcomes, especially cognitive function
Summary
The shift in focus from studying focal pathology to functional brain networks has increased our understanding of the etiology of clinical dysfunction, which is especially relevant in multiple sclerosis (MS). (Mollison et al, 2017; Schoonheim et al, 2014; Schoonheim et al, 2015) Functional brain network inefficiency result ing from accumulating structural damage varies between individuals, Abbreviations: MS, multiple sclerosis; FC, functional connectivity; MEG, magnetoencephalography; INO, internuclear ophthalmoplegia; EDSS, Expanded Disability Status Scale; Pv/Am, peak velocity divided by amplitude; BNA, Brainnetome Network Atlas; AECc, corrected Amplitude Envelope Correlation.but eventually leads to clinical and cognitive decline in MS. (Schoon heim et al, 2015) Network dysfunction has mainly been studied with functional (f)MRI in MS, a measure of brain function based on levels of oxygenated blood. (Nij Bijvank et al, 2020; Sheehy et al, 2020; Nij Bijvank et al, 2019) Importantly, eye movements are generated by a wide-spread and coor dinated functional network. This network integrates sensory, motiva tional, executive and motor information, which is extensively involved in cognitive function. Results: In MS pro- and anti-saccades were abnormal compared to healthy controls A relationship of saccadic eye movements was found with FC of the oculomotor network, which was stronger for regional than global FC. Conclusions: Impaired saccadic eye movements were related to functional connectivity of the oculomotor network and clinical performance in MS. This study showed that, in addition to global network connectivity, studying regional changes in MEG studies could yield stronger correlations
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