Elsevier

Behavioural Brain Research

Volume 361, 1 April 2019, Pages 65-73
Behavioural Brain Research

Research report
Lateralized inhibition of symmetric contractions is associated with motor, attentional and executive processes

https://doi.org/10.1016/j.bbr.2018.12.034Get rights and content

Highlights

  • We calculated time-frequency EEG correlates associated with mirror movements (MM).

  • Contralateral beta desynchronization correlated with MM on dominant discontinued hand.

  • Alpha and theta (de)synchronizations were found whatever the side of discontinuation.

  • Specific motor and non-specific attentional/executive processes contribute to MM.

Abstract

Mirror movements (MM) refer to involuntary contractions occurring in homologous muscles contralateral to the voluntary movements. In right-handers, greater MM occur in the right hand during movements of the non-dominant left hand than conversely. However, it remains to know if such behavioural asymmetry of MM relies only on motor processes or if it is also related to attentional and executive processes. This study explores MM behavioural asymmetry and its cerebral correlates with electroencephalography in 14 right-handed healthy adults. We investigated the quantity and the intensity of MM and the associated task-related power changes in the beta band over central regions (motor processes), in the alpha band over the parietal regions (attentional processes) and in the theta band over frontal regions (executive processes). Behavioural results revealed greater MM in the right hand when the left hand was active than the reverse. This behavioural asymmetry was associated with asymmetry in the cortical activations over motor areas. Greater MM in the right hand correlated with activation over the contralateral left motor region, revealing that selective inhibition of one hand induced activation of the motor cortex leading to MM. In addition, increased cortical activations over parietal and fronto-mesial regions suggest that an increase of attentional and executive processes is required to inhibit one hand, independently of its side. All in all, this study highlights that side-specific motor and non-side-specific attentional and executive processes are associated to the MM asymmetry.

Introduction

Most activities of daily living require unimanual or bimanual coordinated movements. Symmetrical bimanual movements represent the default coordinative behavior of the central nervous system [1,2]. This phenomenon may be related to mirror movements (MM) that are defined as involuntary contractions occurring in homologous muscles contralateral to voluntary movements, particularly in the distal upper limb muscles [[3], [4], [5]]. MM can interfere with the ability to perform complex asymmetric hand skills, particularly those requiring bimanual coordination [2,6]. Various clinical populations exhibit MM, including individuals with Huntington’s or Parkinson disease, stroke, schizophrenia [5,7], attention-deficit/hyperactivity disorder [8,9] and developmental coordination disorder [10,11]. The clinical significance of MM is that they can be considered as neurological soft signs that reflect underlying neurological dysfunction (e.g., [8,12]). In healthy population, MM are typically observed during childhood but are supposed to decrease gradually during the maturation of the central nervous system [13,14]. However, mirrored electromyographic (EMG) activity can still be recorded in healthy adults during complex rhythmic tasks [15,16] or tasks requiring to perform low or high force levels [17,18]. MM reappear more obviously in elderly people compared to younger adults [[19], [20], [21], [22], [23], [24]].

According to the so-called “bilateral activation” theory [25], the mechanism underlying MM in healthy adults is transcallosal facilitation, whereby activation of the motor areas in one hemisphere during voluntary movement facilitates the activation of the same motor areas in the opposite hemisphere [5]. Thus, MM in healthy adults originate in the hemisphere contralateral to the involuntary movement [5,26]. On this basis, the level of MM is determined by the interactions of excitatory and inhibitory neural processes [5,27]. This is consistent with electroencephalographic (EEG) studies showing that execution of unimanual movements is accompanied by bilateral motor activations over the central regions [[28], [29], [30], [31]].

Most of studies indicate a larger occurrence of MM on the dominant hand during voluntary movements of the non-dominant hand, in particular in right-handers [3,18,[32], [33], [34], [35], [36], [37]]. It would seem that such asymmetry of MM depends particularly on the characteristics of movement parameters [38], which could explain that one study reported the reverse pattern [25] and that others failed to find differences in the extent of MM between contractions of the dominant or non-dominant hand [19,20,[38], [39], [40]]. As proposed by Todor and Lazarus, asymmetry of MM between right and left hands in right-handers could be related to differences between hemispheric control of each hand [35]. However, the integration of neural mechanisms underlying this behavioural asymmetry remains to be fully understood. A relevant paradigm to answer this question is the switching motor task, which requires discontinuation of symmetric bimanual rhythmic movements to continue unimanual rhythmic movements with one hand [[41], [42], [43], [44]]. This task evaluates MM in the sense that excitatory processes are mainly involved in symmetric bimanual movements [45] whereas inhibitory processes would be involved for unimanual movement in order to suppress MM on the contralateral limb [7]. At a behavioural level, in accordance with the asymmetry of MM, the study of Tallet et al. [43] showed that right-handed children (7–10 years old) stopped their left finger better than their right one during switching task in bimanual tapping. At a neural level, a study in young adults did not find electro-cortical differences between left and right discontinuations [41] while other EEG studies showed that the left dominant hemisphere is predominant for the motor control [[45], [46], [47], [48]]. Moreover, a global increase of attentional activations has been found independently of the hand stopped, which has been interpreted as the reflect of an “effort” of inhibition of the symmetric movements [41,44]. Finally, the inhibition of symmetric movements is linked with executive control independently of the hand stopped [49]. This suggests that inhibition of MM induces motor, attentional and executive activations but, to date, there is no evidence of cerebral asymmetry to account for behavioural asymmetry, that is, greater MM in the right dominant hand.

On this basis, we propose to use the switching motor task in order to assess the behavioural and brain electro-cortical asymmetries of MM and the related processes in right-handed healthy adults. For each limb (right and left), MM are assessed by EMG peaks on the discontinued hand after motor switching and brain activity was recorded by EEG.

Previous studies on brain activity revealed reduced oscillatory activity over motor cortical areas in the beta frequency band (13–30 Hz) during voluntary contraction, which can be interpreted as an electrophysiological correlate of cortical activations involved in production of motor behavior [29,50]. In addition, beta oscillatory brain activity over motor cortical areas may be involved in the active inhibition of sensorimotor processes and reflect the maintenance of the status quo [51,52]. Interestingly, oscillatory brain activity in the alpha frequency band (8–12 Hz) has been associated with the cortical activation level of the underlying brain areas with low power considered as cortical activation and high power as cortical deactivation or inhibition [[53], [54], [55], [56]]. More specifically, alpha power changes over parietal areas would be more related to cortical activation involved in attentional process and the release from inhibition [53,54]. Finally, oscillatory brain activity in the theta frequency band (4–8 Hz) is increased over fronto-mesial areas during response inhibition paradigms [57] and has been proposed to reflect the cortical activation involved in cognitive control and response inhibition [58].

In order to unravel the contributions of motor, attentional and executive processes in the production of MM, post- (vs pre-) switching EEG task-related power changes are assessed in the beta, alpha and theta bands frequency over the motor, parietal and fronto-mesial cortical areas, respectively [29,50,58,59]. We hypothesize that right-handed healthy adults will present more MM on their right limb during left unilateral voluntary contractions than the reverse, in association with lower task-related power in beta frequency band over left motor area. In alpha frequency band, we expect to find a change of the task-related power over parietal areas after transition (i.e. after discontinuation of one hand contraction). Finally, in theta frequency band, we hypothesize that task-related power over fronto-mesial areas increases after transition.

Section snippets

Participants

Fourteen right-handed healthy adults (3 men and 11 women; mean age: 21.8 ± 1.5 years) participated in the study. All participants were right-handed as assessed by the Edinburgh inventory [60]; mean laterality quotient: 90 ± 13%) and had no known neurological or sensorimotor deficits. All participants were naïve about the hypothesis tested in order to avoid any strategy or attentional focus on the discontinued hand. All participants received explicit information about the experimental design and

Behavioural results: quantity and intensity of MM

Statistical analyses revealed only a significant effect of Side of discontinuation on the number of EMG peaks of the discontinued hand (t13 = 1.84; p = 0.04; d = 0.26). The quantity of MM was significantly higher on the right discontinued hand (83 ± 38) during the right side of discontinuation compared to the left discontinued hand during left side of discontinuation (73 ± 39) (Fig. 5a). In contrast, the intensity of MM was not different between the right and the left discontinued hand (t13

Discussion

The purpose of the present study was to investigate the behavioural and cerebral asymmetries of MM in right-handed healthy adults. EMG and EEG signals were recorded during a switching motor task requiring to produce bimanual symmetric rhythmic power grip contractions and to stop selectively one hand while continuing the unimanual rhythmic contractions of the other hand. The results show (1) a behavioural asymmetry of MM with a greater quantity of MM on the dominant (right) hand during a

Conclusion

To our knowledge, the present study is the first to highlight a behavioural asymmetry of MM associated with cerebral asymmetry in motor activations. Using a switching motor task, this study revealed a larger quantity of MM in the dominant (right) hand when the left hand was active than the opposite. The increased MM in the right hand correlated with contralateral activations over the left motor region, which was not the case for MM in the left hand and contralateral right motor cortex. Hence,

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