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

Abstract

Multiple sclerosis (MS) is a demyelinating disease that results in a broad array of symptoms, including impaired motor performance. How such demyelination of fibers affects the inherent neurophysiological activity in motor circuits, however, remains largely unknown. Potentially, the movement errors associated with MS may be due to imperfections in the internal model used to make predictions of the motor output that will meet the task demands. Prior magnetoencephalographic (MEG) and electroencephalographic brain imaging experiments have established that the beta (15-30 Hz) oscillatory activity in the sensorimotor cortices is related to the control of movement. Specifically, it has been suggested that the strength of the post-movement beta rebound may indicate the certainty of the internal model. In this study, we used MEG to evaluate the neural oscillatory activity in the sensorimotor cortices of individuals with MS and healthy individuals during a goal-directed isometric knee force task. Our results showed no difference between the individuals with MS and healthy individuals in the beta activity during the planning and execution stages of movement. However, we did find that individuals with MS exhibited a weaker post-movement beta rebound in the pre/postcentral gyri relative to healthy controls. Additionally, we found that the behavioral performance of individuals with MS was aberrant, and related to the strength of the post-movement beta rebound. These results suggest that the internal model may be faulty in individuals with MS. Hum Brain Mapp 38:4009-4018, 2017. © 2017 Wiley Periodicals, Inc.

Oscillatory dynamics in the dorsal and ventral attention networks during the reorienting of attention

“…Finally, with regards to the impact of motor‐related responses on our results, at a reviewer's request we imaged the beta response using a shorter time window (i.e., from 300 to 700 ms) than that utilized in our original analysis (i.e., from 300 to 900 ms) to reduce possible contamination by motor‐related activity. While assessing the contribution of motor‐related activity was not a goal of the present study, our laboratory has a history of investigating the oscillatory signature of motor control (Arpin et al, ; Heinrichs‐Graham, Arpin, & Wilson, ; Heinrichs‐Graham et al, ; Heinrichs‐Graham, Santamaria, Gendelman, & Wilson, ; Heinrichs‐Graham & Wilson, ; Kurz, Becker, Heinrichs‐Graham, & Wilson, ; Kurz et al, ; Kurz, Proskovec, Gehringer, Heinrichs‐Graham, & Wilson, ; Wilson et al, ; Wilson, Heinrichs‐Graham, & Becker, ), and we are acquainted with the impact that motor‐related responses can have on cognitive paradigms. As such, we anticipated that beamforming a shorter time window would result in a global reduction in beta power throughout the cortex.…”

Older Age Increases the Amplitude of Muscle Stretch-Induced Cortical Beta-Band Suppression But Does not Affect Rebound Strength

“…Recently, understanding of the factors influencing beta suppression and rebound amplitude has increased with studies showing that certain factors reduce the amplitude of the rebound, such as childhood (Gaetz et al, 2010), demyelination (Arpin et al, 2017), ischemia (Cassim et al, 2001), and stroke (Laaksonen et al, 2012). It has been speculated that the strength of beta rebound reflects the active inhibition or reduced excitability of the SM1 cortex (Pfurtscheller, 1992;Salmelin et al, 1995) and is a GABA-mediated process (Muthukumaraswamy et al, 2013).…”

“…It has been speculated that the strength of beta rebound reflects the active inhibition or reduced excitability of the SM1 cortex (Pfurtscheller, 1992;Salmelin et al, 1995) and is a GABA-mediated process (Muthukumaraswamy et al, 2013). Interestingly, weaker rebound has been linked with worse force accuracy (Arpin et al, 2017) and impaired hand dexterity (Laaksonen et al, 2012). Additionally, stronger rebound is associated with better recovery after stroke (Parkkonen et al, 2017).…”

White matter plasticity and maturation in human cognition

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