Compromised motor imagery ability in individuals with multiple sclerosis and mild physical disability: An ERP study

Abstract

Background

Motor imagery (MI) impairment has been reported in individuals with multiple sclerosis (MS). The present study was designed to investigate neural evidence for MI impairment and its relationship to working memory in MS patients.

Methods

The study participants included 24 early stage MS patients (age: 22–40/mean = 32.7 years; M/F = 4/20; years since duration: 1–10/mean = 5.8) and 24 age-, gender-, and education-matched controls (age: 21–40/mean = 31.8 years; M/F = 5/19). Event-related potentials were recorded during a mental hand rotation task, in which participants were instructed to judge the laterality of hands displayed in different orientations. Furthermore, the Paced Auditory Serial Addition Test (PASAT) was used for assessment of working memory.

Results

At the behavioral level, MS patients were significantly less accurate and much slower (accuracy: 83.80 ± 7.72%; reaction time: 1665.95 ± 269.82 ms) than controls (accuracy: 88.35 ± 7.68%; reaction time: 1505.16 ± 225.11 ms). At the neural level, MS patients showed a significantly reduced amplitude (MS: 0.99 ± 0.89 μv, controls: 1.46 ± 1.00 μv) and delayed peak latency (MS: 458.45 ± 67.60 ms, controls: 417.91 ± 62.47 ms) at P3 for mental rotation effect. Moreover, there were significant correlations between individuals’ PASAT scores and performance of the hand rotation task.

Conclusion

The results of the present study demonstrate MI impairment in patients with MS at both the behavioral and neural level. Neuronal activity dysfunction (decreased and delayed activity) in patients with MS provides new insights into MI impairment. Furthermore, our findings suggest the contribution of working memory dysfunction to compromised MI ability in patients with MS.

Introduction

Motor imagery (MI) is a specific type of mental imagery described as mental rehearsal of a motor act without overt motor output [1]. MI has recently been considered as a therapeutic tool in patients with motor dysfunction who are trying to regain motor skills lost or impaired by neurological diseases [2], [3]. However, impairment of MI ability has also been reported in certain neurological diseases (e.g. stroke and Parkinson's disease) [4], [5] by involving motor, cognitive or somato-sensory function [6]. The lack of MI ability in stroke and slowness of MI in Parkinson disease may be explained by the location of their brain lesions.

Multiple sclerosis (MS) is one of the most common diseases of the central nervous system. It is characterized by demyelination and axonal degeneration, leading to interruption of neuronal connections (termed multiple disconnection syndrome) [7]. Neural disconnection can result in motor as well as cognitive dysfunction. MS is categorized into relapsing-remitting (RRMS, the most frequent subtype), secondary progressive (SPMS), and primary progressive (PPMS). Heremans et al. have recently shown compromised MI ability (lowered accuracy and dysfunction in temporal organization) in patients with MS at different stages of the disease [8]. In addition, Heremans et al. investigated patients’ imagined performance by using eye-movement registration and found temporal and spatial problem during imagined movement [9]. However, to date, no study has investigated neural processing during performance of MI by patients with MS.

Motor imagery is usually studied using Parson's hand rotation paradigm, in which participants judge the laterality of pictures held in either hand at different rotation angles [10]. In general, reaction times and error rates are amplified with increasing angles of rotation, indicating that participants engage in a mental rotation cognitive process. Behavioral studies have shown that mental rotation of the body parts appears to be constrained by the biomechanical properties of physical rotation [11].

Event-related potential (ERP) studies have shown that the mental rotation process is reflected in a modulated positive wave of about 300–700 ms, with decreasing amplitudes for increasing angles of rotation [12]. This slow decrease in amplitude is assumed to be the result of a superimposed negativity on the concurrently prevailing P300 complex, so-called rotation-related negativity (RRN). RRN is considered as an electrophysiological correlate of the mental rotation process, reflecting a stronger neural activity in the parietal cortex and is most pronounced at the P3 and P4 electrodes [13]. One study of patients with right hemiparetic cerebral palsy reported impaired MI ability, reflected in reduced amplitude and increased latency of RRN in patients [14]. Decreased amplitudes and increased latencies of late ERP components have been reported in MS patients, using different cognitive tasks [15]. Nevertheless, the question remains whether impaired MI in MS patients would be demonstrated by alteration of RRN in the mental hand rotation task.

Cognitive impairment (CI) is observed in up to 65% of patients with MS [16]. Domains most affected are attention, speed of information processing, and working memory [7]. Deficient working memory is found in the early stages of MS, when other CIs are subtle. Notably, working memory is crucial among the cognitive processes involved in MI [17], [18] and studies have shown the association between working memory and MI ability [8], [19]. Therefore, the relationship between the ERP characteristics of MS patients during the hand rotation task and their working memory function (assessed by Paced Auditory Serial Addition Test, PASAT) is of interest.

In summary, the present study aimed to assess RRN during the performance of MI and its relation to working memory in patients with MS. For the purposes of this study, the performance of a group of MS patients with mild disability was compared with that of a group of healthy matched controls (CTL) on a mental hand rotation task, while simultaneously measuring encephalograms (EEGs).