Abnormal task driven neural oscillations in multiple sclerosis: A visuomotor MEG study

Abstract

Multiple sclerosis (MS) is a debilitating disease commonly attributed to degradation of white matter myelin. Symptoms include fatigue, as well as problems associated with vision and movement. Although areas of demyelination in white matter are observed routinely in patients undergoing MRI scans, such measures are often a poor predictor of disease severity. For this reason, it is instructive to measure associated changes in brain function. Widespread white-matter demyelination may lead to delays of propagation of neuronal activity, and with its excellent temporal resolution, magnetoencephalography can be used to probe such delays in controlled conditions (e.g., during a task). In healthy subjects, responses to visuomotor tasks are well documented: in motor cortex, movement elicits a localised decrease in the power of beta band oscillations (event-related beta desynchronisation) followed by an increase above baseline on movement cessation (post-movement beta rebound (PMBR)). In visual cortex, visual stimulation generates increased gamma oscillations. In this study, we use a visuomotor paradigm to measure these responses in MS patients and compare them to age-and gender-matched healthy controls. We show a significant increase in the time-to-peak of the PMBR in patients which correlates significantly with the symbol digit modalities test: a measure of information processing speed. A significant decrease in the amplitude of visual gamma oscillations in patients is also seen. These findings highlight the potential value of electrophysiological imaging in generating a new understanding of visual disturbances and abnormal motor control in MS patients. Hum Brain Mapp 38: 2441-2453, 2017.

White matter plasticity and maturation in human cognition

“…By comparing such a clinical population to typically developing children, we were able to reveal differences within neural synchrony—providing a platform to model the impact of myelin and axonal damage across different diseases on neural oscillations during development. Our findings are consistent with findings in adults with MS, where gamma disruption have been observed using MEG during visual task performance (Barratt et al, ; Stickland et al, ). Gamma oscillations may reflect neural input to visual cortex from the retina via the lateral geniculate nucleus (Castelo‐Branco, Neuenschwander, & Singer, ; Sadakane et al, ; Solomon, Lee, & Sun, ).…”

“…Recently, Murty, Shirhatti, Ravishankar, and Ray () demonstrated in humans using EEG and nonhuman primates using local field potentials that slow (~20–40 Hz) gamma emulated long‐range processing and fast (40–70 Hz) gamma was systematic to short‐range processing. (Barratt et al, ; Stickland et al, ). Our findings may reflect core deficits in visual processing that may influence broader cognition in children and adolescents with MS and MOG‐associated disorders—and appear to reflect disrupted local neural communication.…”

“…Cognitive impairment in childhood (Amato et al, 2016;Julian et al, 2013) and later on in adulthood (Ruano et al, 2018) in these patients may be the result of disturbed neural communication due to white and grey matter injury (Arrondo et al, 2009). In that regard, disrupted gamma oscillations are observed in adults with MS (Arpin et al, 2017;Barratt et al, 2017;Stickland et al, 2018). Gamma (30-150 Hz) oscillations are critical for local and large-scale cortical processing (Bastos, Briggs, Alitto, Mangun, & Usrey, 2014;Fries, 2009;Roberts et al, 2013), are associated with higher-order cognitive processes such as perception (Beauchamp, Sun, Baum, Tolias, & Yoshor, 2012;Tallon-Baudry, Bertrand, Delpuech, & Permier, 1997;Tallon-Baudry, Bertrand, Delpuech, & Pernier, 1996), attention (Chalk et al, 2010;Fries, Reynolds, Rorie, & Desimone, 2001;Marshall, O'Shea, Jensen, & Bergmann, 2015;Womelsdorf & Fries, 2007), and processing of sensory stimuli (Cheyne, Bells, Ferrari, Gaetz, & Bostan, 2008) and are disturbed in psychiatric disorders (Grützner et al, 2013).…”

Altered sensorimotor cortical oscillations in individuals with multiple sclerosis suggests a faulty internal model

“…In our study, individuals with MS exhibited a weaker PMBR in the pre‐ and post‐central gyri relative to healthy individuals. Similar findings were previously reported in an EEG study of self‐paced movements of the hand in individuals with MS [Leocani et al, ], and abnormal PMBR responses were also detected in a recent MEG study of visuomotor performance involving the hands of patients with MS [Barratt et al, ]. Together, these results provide mounting evidence that the PBMR response is disturbed in individuals with MS.…”

Estimation of narrowband amplitude and phase from electrophysiology signals for phase-amplitude coupling studies: a comparison of methods

“…It would also be necessary to deal adequately with methodological issues that may prevent the correct identification of brain behavior with the available PAC methods (Aru et al, 2015), such as number of filters and their passband width, non-stationarity, and influence of signal power fluctuations in PAC modulations -in section 3.3, our goal with the VM data was essentially to observe the impact of the choice of approach with real MEG measurements. That being said, it should be pointed out that the some of the experimental outcomes of the present article coincide with other investigations dealing with the implications of visuomotor coordination in brain electrical activity: for instance, there is evidence of increased delta (Jerbi et al, 2007;Bradberry et al, 2009;Bourguignon et al, 2012;Mylonas et al, 2016) and gamma activity (Brovelli et al, 2017) in the motor cortex, and of gamma activity in the visual cortex (Barratt et al, 2017). Again, further analysis is necessary to better link our findings with those that appeared in the literature, particularly because the latter did not necessarily involve PAC computations.…”