The Neurophysiological Impact of Subacute Stroke: Changes in Cortical Oscillations Evoked by Bimanual Finger Movement

ntroduction. To design more effective interventions, such as neurostimulation, for stroke rehabilitation, there is a need to understand early physiological changes that take place that may be relevant for clinical monitoring. We aimed to study changes in neurophysiology following recent ischemic stroke, both at rest and with motor planning and execution. Materials and Methods. We included 10 poststroke patients, between 7 and 10 days after stroke, and 20 age-matched controls to assess changes in cortical motor output via transcranial magnetic stimulation and in dynamics of oscillations, as recorded using electroencephalography (EEG). Results. We found significant differences in cortical oscillatory patterns comparing stroke patients with healthy participants, particularly in the beta rhythm during motor planning () and execution () of a complex movement with fingers from both hands simultaneously. Discussion. The stroke lesion induced a decrease in event-related desynchronization in patients, in comparison to controls, providing evidence for decreased disinhibition. Conclusions. After a stroke lesion, the dynamics of cortical oscillations is changed, with an increasing neural beta synchronization in the course of motor preparation and performance of complex bimanual finger tasks. The observed patterns may provide a potential functional measure that could be used to monitor and design interventional approaches in subacute stages.

1. Introduction
Stroke represents the third major cause of death and is one of the leading sources of disability, contributing to a decline in the global quality of life. Although several approaches are applied to the rehabilitation of patients, current interventions lack efficacy [1].

In order to develop new and more effective interventions for neurorehabilitation, and particularly, for the rehabilitation of stroke patients, it is fundamental to understand subacute physiological changes of potential neuroplastic significance following the event. After a brain lesion, neural networks are damaged, which triggers the reorganization of neural connectivity and brain rhythms. Plastic changes may occur not only on the lesioned but also in the contralateral hemisphere [2]. It is frequently reported in the literature that the activity of the unaffected hemisphere increases in the first days after the cerebrovascular accident [2, 3]. After this period, at 3 to 6 months following the event, a relative increase in the activity of the areas adjacent to the lesion is frequently observed, concurrent with functional improvements [3].

Functional techniques to assess brain changes include electroencephalography, magnetoencephalography, and functional magnetic resonance imaging [2]. Electroencephalography (EEG) can potentially contribute to the understanding of the physiology of brain reorganization [4], in particular in which concerns the study of dynamics of oscillations [5].

Brain oscillations can appear at diverse frequencies, associated to distinct levels of synchrony in neuronal networks [6]. The visual alpha rhythm is known to respond to a stimulus or instruction with a decrease in amplitude or power, resulting in an event-related desynchronization (ERD). Synchronization (ERS) occurs in the absence of stimuli or idle states. It is therefore believed that alpha ERS is associated to cortical inhibition, whereas ERD is related to the reduction of inhibition, in turn [7]. Current knowledge, nevertheless, also points out a role for other types of alpha rhythm in attention and conscious awareness [8].

Performing a voluntary movement or receiving instructions to execute a motor task are generally associated with a decrease in upper alpha (mu rhythm) and in beta rhythms [6, 7], in those regions around sensorimotor areas [6, 9]. This reduction of movement-related beta power is thought to be associated with the excitability of the primary motor cortex and to be affected by GABA (gamma-aminobutyric acid) levels [10].

Preparation and execution of motor tasks might reveal altered activity patterns in stroke, which may have significant implications for the design of therapeutic interventions [11]. Changes in neural synchronization and oscillatory activities can play a role in the pathophysiology of distinct disorders, such as in stroke [7]. The poststroke changes in brain oscillations, particularly those accompanying movements of the impaired limbs, are worthy of further research [10]. Therefore, exploration of biomarkers to strengthen stroke investigation has been advocated [12], and recent works have been studying EEG activity in stroke, along with motor tasks, such as unilateral [11–13] or bilateral wrist movements [13].

Here, we determined motor thresholds as a measure of cortical excitability and assessed ERD and ERS in the course of motor tasks, both in healthy subjects and in poststroke patients. To the best of our knowledge, this is the first time that the neurophysiology of stroke patients is analysed shortly after the event (between 7 and 10 days poststroke) by EEG preceding and during simple and complex fine-tuned unilateral and bilateral motor tasks performed with both the affected and unaffected arms and hands, and a direct comparison with a control healthy sample that did the same experiment is provided. Our aim was to study the impact of a subacute ischemic stroke in brain neurophysiology at rest and during motor preparation and execution. Moreover, we investigated whether significant changes in the EEG brain activity pattern following stroke could be correlated with the motor performance of the affected upper limb, assessed by the Wolf Motor Function Test.