Gait initiation is preceded by initial postural adjustments whose goal is to set up the condition required for the execution of the focal stepping movement. For instance, the step is preceded by a shift of the body’s center of mass towards the stance foot unloading the stepping leg. This displacement is produced by exerting forces on the ground (i.e., thrust) while the body is still motionless. The purpose of this study was to identify whether the mere cutaneous inputs from the feet soles evoked by a lateral translation of the support could be used to scale the initial postural adjustments. Participants stood with their eyes closed on a force platform that could be moved laterally with a low acceleration (between 0.14 m/s2 and 0.30 m/s2) to reach a constant velocity of 0.02 m/s. This translation resulted in a change in the somatosensory cues from the feet soles without modifying vestibular inputs. Participants were instructed to produce a step with the right foot as soon as they felt the platform start to move (on either side) or heard an auditory cue. In the latter case, the platform stayed stationary. We found that the thrust duration was lengthened when the platform moved towards the supporting foot. In this condition, the cutaneous stimulation provided information related to a body shift towards the stepping leg. This increased thrust duration likely helped overcoming the non-functional body shift perceived towards the stepping leg. This result highlights the accuracy with which the actual standing position can be determined from foot sole cutaneous cues in the absence of visual and vestibular or proprioceptive inputs.
It has been shown that during the planning of a voluntary movement the transmission of cutaneous afferent inputs to the somatosensory cortex is attenuated shortly before the motor output as well as during movement execution. However, it is not known whether the sensory suppression observed during the planning phase (i.e., before any movement execution) is a systemic phenomenon or whether it is dependent on movement context. For example, movements such as step initiation are controlled based on information received from cutaneous receptors in the feet. Because afferent information emerging from these receptors is critical for movement initiation, we hypothesized that suppression of these inputs may not occur during the planning phase prior to gait initiation. To examine this hypothesis we measured the cortical response to somatosensory stimulation during the planning phase of step initiation and during movement execution. Sensitivity to cutaneous stimulation was assessed by measuring the amplitude of the cortical somatosensory-evoked potential (SEP, over the Cz electrode) following electrical stimulations of the plantar sole of one foot. Two stimulations were provided during the planning phase of a step movement and two stimulations during movement execution. It was found that the P50-N80 SEP was facilitated in the early planning phase (−700 ms before motor execution) compared with when participants remained still (control standing task). This mechanism might contribute to an enhanced perception of cutaneous input leading to a more accurate setting of the forces to be exerted onto the ground to shift the body's weight toward the supporting side prior to foot-off.
Previous studies on the control of human balance suggested that increased pressure under the feet, leading to reduced plantar sole mechanoreceptors sensitivity, increases body sway. Although this suggestion is attracting, it is unclear whether increased plantar sole pressure simply reduces the transmission of plantar sole afferent to the cortex or also alters the sensorimotor integrative mechanisms. Here we used electrical stimulation applied under the sole of the foot to probe the sensorimotor mechanisms processing foot mechanoreceptors. Balance control of healthy individuals was assessed either when wearing a loaded vest or in normal-weight condition. In the Loaded condition, we observed decreased cortical activity over the primary somatosensory cortex for both an early P50-N90 somatosensory evoked potential (SEP) and, for oscillatory brain activity within the gamma band (30-80 Hz). These reductions were interpreted as a disrupted early sensory transmission (i.e., decreased early SEP) leading to a decreased perception of plantar sole sensory information (i.e., decreased gamma band power). These early sensory mechanisms for the Loaded condition were associated with an increase in the late P170-N210 SEP and oscillatory brain activity within the beta band (19-24 Hz). These neural signatures involved areas which are engaged in sensorimotor integrative processes (secondary somatosensory cortex and right temporoparietal junction). Altered early and late sensory processes may result from the increase pressure on the mechanoreceptors of the foot sole and not from postural instability per se. Indeed, postural instability with normal weight condition did not lead to SEP changes.
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.
28 December 2020 in Cerebral Cortex Communications
Cutaneous foot receptors are important for balance control, and their activation during quiet standing depends on the speed and the amplitude of postural oscillations. We hypothesized that the transmission of cutaneous input to the cortex is reduced during prolonged small postural sways due to receptor adaptation during continued skin compression. Central mechanisms would trigger large sways to reactivate the receptors. We compared the amplitude of positive and negative post-stimulation peaks (P50N90) somatosensory cortical potentials evoked by the electrical stimulation of the foot sole during small and large sways in 16 young adults standing still with their eyes closed. We observed greater P50N90 amplitudes during large sways compared with small sways consistent with increased cutaneous transmission during large sways. Postural oscillations computed 200 ms before large sways had smaller amplitudes than those before small sways, providing sustained compression within a small foot sole area. Cortical source analyses revealed that during this interval, the activity of the somatosensory areas decreased, whereas the activity of cortical areas engaged in motor planning (supplementary motor area, dorsolateral prefrontal cortex) increased. We concluded that large sways during quiet standing represent self-generated functional behavior aiming at releasing skin compression to reactivate mechanoreceptors. Such balance motor commands create sensory reafference that help control postural sway.
Somatosensory inputs to the cortex undergo an early and a later stage of processing which are characterized by an early and a late somatosensory evoked potentials (SEP). The early response is highly representative of the stimulus characteristics whereas the late response reflects a more integrative, task specific, stage of sensory processing. We hypothesized that the later processing stage is independent of the early processing stage. We tested the prediction that a reduction of the first volley of input to the cortex should not prevent the increase of the late SEP. Using the sensory interference phenomenon, we halved the amplitude of the early response to somatosensory input of the ankle joints (evoked by vibration) when participants either planned a step forward or remained still. Despite the initial cortical response to the vibration being massively decreased in both tasks, the late response was still enhanced during step planning. Source localization indicated the posterior parietal cortex (PPC) as the likely origin of the late response modulation. Overall these results support the dissociation between the processes underlying the early and late SEP. The later processing stage could involve both direct and indirect thalamic connections to PPC which bypass the postcentral somatosensory cortex.