Corticospinal responses of quadriceps are abnormally coupled with hip adductors in chronic stroke survivors

Abstract

Stroke survivors often lose the ability to move their joints independently, which results in abnormal movement patterns when attempting to perform an isolated motion. For instance, many stroke subjects exhibit unwanted secondary knee extension movement when performing hip adduction. This study aimed at characterizing whether the neural substrates mediating abnormal activation patterns after stroke are of cortical origin. We developed a novel transcranial magnetic stimulation protocol to evaluate the extent of abnormal across-joint coupling of corticospinal responses in chronic stroke survivors. In stroke survivors, we found that the magnitude of motor evoked potentials of the vastus lateralis and vastus medialis during isometric hip adduction were significantly higher than those recorded during knee extension at similar background activity (P = 0.03 and P = 0.01). Moreover, motor evoked potential coupling ratios of the quadriceps muscles were significantly different than those observed in healthy controls (P = 0.005 to P = 0.037). No differences in motor evoked potential coupling ratios were observed between the younger and older adults (P = 0.474 to P = 0.919). These findings provide evidence for the first time that stroke subjects exhibit abnormal excitability of the quadriceps muscle corticospinal neurons when performing isometric hip adduction. Importantly, the abnormal corticospinal responses observed in stroke subjects were not mediated by aging. The results of this study provide new insights into the mechanisms underlying loss of independent joint control after stroke and have meaningful implications for post-stroke interventions. Moreover, the proposed ‘motor evoked potential coupling ratio’ may serve as an effective probe to evaluate cortical contributions to abnormal muscle synergy after stroke.

Introduction

Loss of independent joint control is one of the most common neuromotor impairments that occur after stroke (Brunnstrom, 1970, Twitchell, 1951). The inability to perform movements in an isolated fashion results in the emergence of stereotypical movement patterns involving tight coupling of motions across joints (Cruz and Dhaher, 2008, Dipietro et al., 2007). This abnormal across-joint coupling has been shown to exist in both upper and lower extremities, irrespective of whether the task is static or dynamic (Cruz and Dhaher, 2008, Dipietro et al., 2007, Schwerin et al., 2008). Interestingly, these abnormal stereotypical movement/torque patterns are known to correlate with the loss of functional ability in stroke survivors (Cruz et al., 2009). As a result, an understanding of the mechanisms that contribute to abnormal across-joint coupling may assist in identifying appropriate neurophysiological targets for functional recovery in stroke.

While there is compelling evidence for the presence of tight coupling of motions across joints, the mechanisms that mediate such movement patterns remain poorly understood. One possible mechanism may be that the structural reorganization of the brain following stroke can be maladaptive. The structural changes that occur after stroke are often characterized by axonal sprouting of undamaged intracortical and interhemispheric neuronal projections to the damaged regions of the brain (Carmichael, 2003, Carmichael, 2008, Carmichael et al., 2005). Although this plasticity mediates functional recovery, the new neural networks that are established during the process of reorganization may also result in abnormal connections with negative consequences on neuromotor recovery (Beauchamp and Ro, 2008). Moreover, stroke induced physiological alterations, such as increased cortical overlap of joint representations and decreased cortical spatial resolution for recruiting individual muscles, may affect the output properties of the motor cortex in such a way that it may promote abnormal across-joint coupling (Yao et al., 2009).

It seems reasonable that if the neural substrates of abnormal across-joint coupling are of cortical origin, then the output of the motor cortex (corticospinal responses) when performing a simple isolated task should also be coupled. An observation of such coupled responses will also provide a much stronger evidence for the presence of abnormal neuronal connections in stroke survivors. However, to the best of our knowledge there are no studies that have evaluated whether monohemispheric stroke results in abnormal across-joint coupling of the corticospinal responses. To this end, we examined whether the excitability of the corticospinal neurons of the knee extensor muscle groups when performing an isometric hip adduction task was abnormally modified after stroke. We hypothesized that the stroke subjects would demonstrate abnormal higher corticospinal responses of the quadriceps muscle group during an isometric hip adduction task.