Sound-Evoked Biceps Myogenic Potentials Reflect Asymmetric Vestibular Drive to Spastic Muscles in Chronic Hemiparetic Stroke Survivors

Abstract

Aberrant vestibular nuclear function is proposed to be a principle driver of limb muscle spasticity after stroke. We sought to determine whether altered cortical modulation of descending vestibulospinal pathways post-stroke could impact the excitability of biceps brachii motoneurons. Twelve chronic hemispheric stroke survivors aged 46-68 years were enrolled. Sound evoked biceps myogenic potentials (SEBMPs) were recorded from the spastic and contralateral biceps muscles using surface EMG electrodes. We assessed the impact of descending vestibulospinal pathways on biceps muscle activity and evaluated the relationship between vestibular function and the severity of spasticity. Spastic SEBMP responses were recorded in 11/12 subjects. Almost 60% of stroke subjects showed evoked responses solely on the spastic side. These data strongly support the idea that vestibular drive is asymmetrically distributed to biceps motoneuron pools in hemiparetic spastic stroke survivors. This abnormal vestibular drive is very likely to be a factor mediating the striking differences in motoneuron excitability between the clinically affected and clinically spared sides. This study extends our previous observations on vestibular nuclear changes following hemispheric stroke and potentially sheds light on the underlying mechanisms of post-stroke spasticity.

Keywords: biceps brachii; motoneuron; spastic hypertonia; stroke; vestibular evoked myogenic potential; vestibular reflexes; vestibulospinal.

Figure 1

Central hypothesis. Abnormal excitatory ionotropic drive from descending supraspinal pathways perches the baseline membrane potential of contralesional (clinically affected) motoneurons closer to activation threshold, resulting in the lateralized enhancement of stretch reflex excitability.

Figure 2

Subject positioning and electrode montage used for the collection of SEBMPs. SEBMPs were collected from the tonically active biceps brachii muscles in 12 chronic stroke subjects. Surface electrodes were placed distally on the biceps muscle belly, a third of the distance between the medial acromion and the fossa cubit (interelectrode distance, 25–30 mm). A ground electrode was placed over the epicondyle process. Subjects lay supine on an examination table and were instructed to maintain a moderate isometric contraction in the biceps brachii by pulling against a strap attached to the examination table.

Figure 3

SEBMP waveform analysis. The SEBMP waveform is a stimulus-triggered average generated in response to binaural acoustic stimulation. A peak was labeled p1 if it occurred between 20 and 75 ms and exceeded two standard deviations above baseline based on the prestimulus unrectified EMG (50 ms period). The subsequent peak of opposite polarity immediate following p1 was designated p2. The interpeak amplitude and interpeak interval were calculated from the unrectified waveform average.

Figure 4

Normalized SEBMPs from the CA (A) and CS (B) biceps brachii muscles of chronic stroke subjects. The CA and CS population averages are superimposed (thick line) over the individual responses. For clarity, the individual responses are normalized with respect to p1 (latency).

Figure 5

For the 11 subjects in groups BIL and USPA, there is a weak-positive, but a non-significant relationship between the CA corrected interpeak amplitude and the severity of spasticity in the elbow flexors. The coefficient of determination and p-value are indicated in the upper left of the figure.

Figure 6

BIL and USPA subjects were binned per the severity of spasticity, determined by the antigravity spasticity index (AGSI). Within each bin, subjects were rank-ordered in terms of increasing AR.

Figure 7

Vestibular pathway abnormalities post-stroke. The cerebral cortex exerts powerful control over the vestibular nuclear complex. It is linked to the contralateral MVN and LVN and the ipsilateral SVN by fiber pathways originating in the premotor and vestibular cortices. Our main hypothesis is that the lateralized disruption of corticobulbar projections causes an imbalance in descending vestibular drive to the spinal motoneuron pools, which sets the membrane potential of spastic motoneurons closer to their activation threshold. Here, a lateralized disruption (star) in corticobulbar projections (dashed lines) releases the (a) ipsilateral SVN and the (b) contralateral LVN and MVN as well as their associated ascending and descending pathways from inhibitory cortical control (thick lines). The thickness of the pathway lines represents relative levels of activity within the given pathway. The results of the current study support a lateralized disruption in vestibular pathways post-stroke, especially when added to our previous work.