[ARTICLE] Quantification of task-dependent cortical activation evoked by robotic continuous wrist joint manipulation in chronic hemiparetic stroke – Full Text

Abstract

Background

Cortical damage after stroke can drastically impair sensory and motor function of the upper limb, affecting the execution of activities of daily living and quality of life. Motor impairment after stroke has been thoroughly studied, however sensory impairment and its relation to movement control has received less attention. Integrity of the somatosensory system is essential for feedback control of human movement, and compromised integrity due to stroke has been linked to sensory impairment.

Methods

The goal of this study is to assess the integrity of the somatosensory system in individuals with chronic hemiparetic stroke with different levels of sensory impairment, through a combination of robotic joint manipulation and high-density electroencephalogram (EEG). A robotic wrist manipulator applied continuous periodic disturbances to the affected limb, providing somatosensory (proprioceptive and tactile) stimulation while challenging task execution. The integrity of the somatosensory system was evaluated during passive and active tasks, defined as ‘relaxed wrist’ and ‘maintaining 20% maximum wrist flexion’, respectively. The evoked cortical responses in the EEG were quantified using the power in the averaged responses and their signal-to-noise ratio.

Results

Thirty individuals with chronic hemiparetic stroke and ten unimpaired individuals without stroke participated in this study. Participants with stroke were classified as having severe, mild, or no sensory impairment, based on the Erasmus modification of the Nottingham Sensory Assessment. Under passive conditions, wrist manipulation resulted in contralateral cortical responses in unimpaired and chronic stroke participants with mild and no sensory impairment. In participants with severe sensory impairment the cortical responses were strongly reduced in amplitude, which related to anatomical damage. Under active conditions, participants with mild sensory impairment showed reduced responses compared to the passive condition, whereas unimpaired and chronic stroke participants without sensory impairment did not show this reduction.

Conclusions

Robotic continuous joint manipulation allows studying somatosensory cortical evoked responses during the execution of meaningful upper limb control tasks. Using such an approach it is possible to quantitatively assess the integrity of sensory pathways; in the context of movement control this provides additional information required to develop more effective neurorehabilitation therapies.

Background

The cerebral cortex plays an important role in feedforward (i.e. voluntary motor drive) and feedback control (i.e. reflexes and modulation of spinal reflexes) of human movement [1]. Cortical damage after stroke impairs both feedforward and feedback control. Altered feedforward control after stroke has been thoroughly studied and may lead to motor impairments such as weakness and abnormal synergy-dependent motor control [23].

Cortical involvement in feedback control (including sensorimotor integration and spinal reflex modulation) requires connectivity between somatosensory receptors in the periphery and the sensorimotor cortex, yet compromised integrity of this somatosensory system after stroke has received little attention in the literature. Understanding the impact of sensory impairment, as well as motor impairment, is highly relevant for the development and selection of neurorehabilitation therapies aimed to enhance and normalize motor control [4567] and for evaluating their effectiveness.

Proprioceptive and tactile information are required for feedback control of a joint, and can be studied in an experimental setting by disturbing the joint via a robotic manipulator during motor control tasks. This robotic joint manipulation results in activation of spinal reflex loops [8910] as well as in activation of the somatosensory cortex via high-resolution sensory pathways [11]. However, the cortical activity evoked by joint manipulation and consequently the cortical involvement in feedback control have received less attention.

In able-bodied individuals, evoked cortical responses to robotic joint manipulation have been studied with transient [1213] and continuous disturbances [141516]. Continuous disturbances uninterruptedly provide input to the sensory system, allowing for studying movement control and somatosensory cortical activity during meaningful motor tasks. This study determines the cortical representation of afferent (proprioceptive and tactile) information in individuals with chronic hemiparetic stroke under different upper limb control conditions, relying on objective metrics derived from the electroencephalogram (EEG). Here, the goal is to quantify evoked cortical activation in individuals with chronic hemiparetic stroke, through a combination of robotic continuous joint manipulation of the paretic limb and high-density EEG. The evoked cortical activation reveals the integrity of the connections between sensory receptors in the periphery and the sensorimotor cortices.

It is hypothesized that, due to stroke-induced damage to the somatosensory system, individuals with clinically assessed proprioceptive and tactile impairment will show decreased cortical evoked responses to continuous joint manipulation in the absence of voluntary motor activity of the affected upper limb, as compared to unimpaired persons. In general, when voluntary motor activity of the affected upper limb is required, individuals with hemiparesis have been shown to recruit their contralesional brain hemisphere, i.e. ipsilateral to the movement [17181920]. It is unclear, however, what this recruitment means with regard to somatosensory (i.e. afferent) evoked cortical activity, as the anatomical pathways conducting proprioceptive and tactile information mainly connect to the contralateral hemisphere [21]; thus, increased evoked cortical activation of the ipsilateral hemisphere is not expected.

Continue —> Quantification of task-dependent cortical activation evoked by robotic continuous wrist joint manipulation in chronic hemiparetic stroke | Journal of NeuroEngineering and Rehabilitation | Full Text

Fig. 1 Experimental setup. a The forearm of the participant is strapped into an armrest and the hand is strapped to the handle of the robotic manipulator, requiring no hand force to hold the handle. b Visual feedback as presented to the participant. The circle and crosshairs are always visible. The yellow arrow is only visible during the active task and points up if the target torque is applied. c Close-up of the arm in the robotic manipulator. The wrist joint is aligned with the axis of the motor and is placed in the neutral angle, defined as 20° wrist flexion. d One period of the disturbance signal applied to the wrist (root-mean-square of 0.02 rad). Zero radians corresponds to the neutral angle of the wrist

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