StartReact during gait initiation reveals differential control of muscle activation and inhibition in patients with corticospinal degeneration

Bas J H Van Lith,Jorik Nonnekes,Alexander C Geurts,Milou J M Coppens,Vivian Weerdesteyn,Bart P C Van De Warrenburg

doi:10.1007/s00415-018-9027-0

Abstract

Corticospinal lesions cause impairments in voluntary motor control. Recent findings suggest that some degree of voluntary control may be taken over by a compensatory pathway involving the reticulospinal tract. In humans, evidence for this notion mainly comes from StartReact studies. StartReact is the acceleration of reaction times by a startling acoustic stimulus (SAS) simultaneously presented with the imperative stimulus. As previous StartReact studies mainly focused on isolated single-joint movements, the question remains whether the reticulospinal tract can also be utilized for controlling whole-body movements. To investigate reticulospinal control, we applied the StartReact paradigm during gait initiation in 12 healthy controls and 12 patients with ‘pure’ hereditary spastic paraplegia (HSP; i.e., retrograde axonal degeneration of corticospinal tract). Participants performed three consecutive steps in response to an imperative visual stimulus. In 25% of 16 trials a SAS was applied. We determined reaction times of muscle (de)activation, anticipatory postural adjustments (APA) and steps. Without SAS, we observed an overall delay in HSP patients compared to controls. Administration of the SAS accelerated tibialis anterior and rectus femoris onsets in both groups, but more so in HSP patients, resulting in (near-)normal latencies. Soleus offsets were accelerated in controls, but not in HSP patients. The SAS also accelerated APA and step reaction times in both groups, yet these did not normalize in the HSP patients. The reticulospinal tract is able to play a compensatory role in voluntary control of whole-body movements, but seems to lack the capacity to inhibit task-inappropriate muscle activity in patients with corticospinal lesions.

Highlights

Patients with an upper motor neuron syndrome (UMNS; e.g., stroke, spinal cord injury, cerebral palsy, hereditary spastic paraplegia) have impaired voluntary motor control due to absent or reduced corticospinal output to the alpha motoneurons in the spinal cord
The mean delay in hereditary spastic paraplegia (HSP) patients was significant without a startling acoustic stimulus (SAS), but with a SAS the onsets were no longer different from controls
The SAS-induced acceleration was significantly greater in HSP patients than in the controls (SAS × group, F(1,22) = 6.388, p = 0.019), the delay in rectus femoris (RF) onsets in the HSP patients compared to healthy controls remained significant with a SAS

Summary

Introduction

Patients with an upper motor neuron syndrome (UMNS; e.g., stroke, spinal cord injury, cerebral palsy, hereditary spastic paraplegia) have impaired voluntary motor control due to absent or reduced corticospinal output to the alpha motoneurons in the spinal cord. Volitional movements like gait initiation or reaching while standing are impaired in these patients [36, 49, 52]. Evidence for the potential utility of this compensatory pathway for voluntary movements comes from studies that evaluated the StartReact effect. StartReact refers to the phenomenon that reaction times are greatly accelerated when a startling stimulus is presented simultaneously with an imperative stimulus for executing the requested movement. The exact mechanisms underlying StartReact are, still under debate, as the extent of the reaction time acceleration seems

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