Do gravity-related sensory information enable the enhancement of cortical proprioceptive inputs when planning a step in microgravity?

Abstract

We recently found that the cortical response to proprioceptive stimulation was greater when participants were planning a step than when they stood still, and that this sensory facilitation was suppressed in microgravity. The aim of the present study was to test whether the absence of gravity-related sensory afferents during movement planning in microgravity prevented the proprioceptive cortical processing to be enhanced. We reestablished a reference frame in microgravity by providing and translating a horizontal support on which the participants were standing and verified whether this procedure restored the proprioceptive facilitation. The slight translation of the base of support (lateral direction), which occurred prior to step initiation, stimulated at least cutaneous and vestibular receptors. The sensitivity to proprioceptive stimulation was assessed by measuring the amplitude of the cortical somatosensory-evoked potential (SEP, over the Cz electrode) following the vibration of the leg muscle. The vibration lasted 1 s and the participants were asked to either initiate a step at the vibration offset or to remain still. We found that the early SEP (90-160 ms) was smaller when the platform was translated than when it remained stationary, revealing the existence of an interference phenomenon (i.e., when proprioceptive stimulation is preceded by the stimulation of different sensory modalities evoked by the platform translation). By contrast, the late SEP (550 ms post proprioceptive stimulation onset) was greater when the translation preceded the vibration compared to a condition without pre-stimulation (i.e., no translation). This suggests that restoring a body reference system which is impaired in microgravity allowed a greater proprioceptive cortical processing. Importantly, however, the late SEP was similarly increased when participants either produced a step or remained still. We propose that the absence of step-induced facilitation of proprioceptive cortical processing results from a decreased weight of proprioception in the absence of balance constraints in microgravity.

Figure 1. Experimental set-up and mean lateral platform acceleration (left scale and red curve) and head acceleration (right scale and black curve) during Translation standing condition for the 6 participants.

The onset and offset of head acceleration and deceleration, respectively, were indicated by the arrows according to the vestibular threshold (horizontal dotted lines). B: Mean platform and head accelerations for each of the 6 participants.

Figure 2. SEPs recordings. Grand-Average for 6 participants recorded at electrode Cz for the Stationnary standing condition (Top panel), Translation standing and Translation stepping conditions (Bottom panel).

The vertical dotted lines indicate the vibration onset and offset, the second vertical dotted line also indicates imperative tone stimulus for step execution. For both Translation conditions, the vertical dash-dotted line indicates the translation onset (occurring 500 ms before vibration). The “foot-off” indicates the onset of the stepping movement computed on the foot vertical velocity. The scalp topography was shown at the peak negativity for the participants average in the Sationary and Translation conditions.

Figure 3. Mean P1-N1 SEP amplitude of each participant (P1–P6) for the Stationary and Translation platform conditions (upper panel).

Normalized attenuation for the translation condition relative to the Stationary condition (bottom panel). The mean attenuation for the 6 participants was of 21% (±6). B: Mean amplitudes for 6 participants of the P1-N1 early SEP and mean integral of EEG activity (iEEG, late SEP) computed in a time window comprising between early SEP ending until 600 ms (*: p<0.05).

Figure 4. Results of source reconstruction from the grand average EEG data of the 6 participants (Low Resolution Electromagnetic Tomography, sLORETA) displayed on the used source space (Montreal warp brain aligned to the co-ordinate system of Talairach and Tournaux).

sLORETA images depicted the estimated current density strengh corresponding to the effect of translation relative to baseline (Translation minus Stationary) for the Late SEP. The scale of the maps was chosen to maximize identification of the sources and were given a marked threshold to only show source activity that was 18% upper of minimal activation. Note the clearly distinguishable activation above the primary somatosensory cortice (top view) and the right posterior parietal cortex (e.g., VIP) and the Temporoparietal region.