Supplementary Motor Area and Superior Parietal Lobule Restore Sensory Facilitation Prior to Stepping When a Decrease of Afferent Inputs Occurs

Abstract

The weighting of the sensory inputs is not uniform during movement preparation and execution. For instance, a transient increase in the transmission to the cortical level of cutaneous input ~700 ms was observed before participants initiated a step forward. The sensory facilitation occurred at a time when feet cutaneous information is critical for setting the forces to be exerted onto the ground to shift the center of mass toward the supporting side prior to foot-off. Despite clear evidence of task-dependent modulation of the early somatosensory signal transmission, the neural mechanisms are mainly unknown. One hypothesis suggests that during movement preparation the premotor cortex and specifically the supplementary motor area (SMA) can be the source of an efferent signal that facilitates the somatosensory processes irrespectively of the amount of sensory inputs arriving at the somatosensory areas. Here, we depressed mechanically the plantar sole cutaneous transmission by increasing pressure under the feet by adding an extra body weight to test whether the task-dependent modulation is present during step preparation. Results showed upregulation of the neural response to tactile stimulation in the extra-weight condition during the stepping preparation whereas depressed neural response was still observed in standing condition. Source localization indicated the SMA and to a lesser extent the superior parietal lobule (SPL) areas as the likely origin of the response modulation. Upregulating cutaneous inputs (when mechanically depressed) at an early stage by efferent signals from the motor system could be an attempt to restore the level of sensory afferents to make it suitable for setting the anticipatory adjustments prior to step initiation.

Keywords: balance control; body representation in brain; somatosensory evoked potential; step movement; supplementary motor area (SMA).

Figure 1

(A, left panel) Behavioral recordings during the Stepping task for one representative participant: mediolateral center of pressure, and foot movement in dotted line. Electric stimulations during motor preparation was identified. (A, right panel) The 20 kg weight was distributed on the front and back of the vest. (B, left panel) Grand average somatosensory-evoked potential (SEP). Dashed line indicates the moment of the stimulation. Note that the first potential observed −300 ms prior to the electrical stimulus was an auditory potential evoked by the pre-cue tone. (B, right panel) Mean amplitude for 15 participants of the averaged P₅₀-N₉₀ SEP evoked by the electrical stimulation and recorded over Cz electrode during Standing (St0) and movement preparation (St1 and St2). (^*p < 0.05 and ^**p < 0.01).

Figure 2

Statistical source estimation maps for St1vs. St0 contrast (i.e., Stepping minus Standing tasks) in the Loaded condition. Significant t-values (p ≤ 0.05, n = 15) of the source localization during the [50–90 ms] and [90–130 ms] time windows projected on a cortical template (MNI's Colin 27). For both windows we display the top cortical view and the internal view of the left hemisphere for the P₅₀-N₉₀ SEP. The red color represents a higher activity in St1 relative to St0.