Chapter 5 - The Foot to Brain Connection.pdf (original) (raw)
Proprioceptive information from the foot/ankle provides important information regarding body sway for balance control, especially in situations where visual information is degraded or absent. Given known increases in catastrophic injury due to falls with older age, understanding the neural basis of proprioceptive processing for balance control is particularly important for older adults. In the present study, we linked neural activity in response to stimulation of key foot proprioceptors (i.e., muscle spindles) with balance ability across the lifespan. Twenty young and 20 older human adults underwent proprioceptive mapping; foot tendon vibration was compared with vibration of a nearby bone in an fMRI environment to determine regions of the brain that were active in response to muscle spindle stimulation. Several body sway metrics were also calculated for the same participants on an eyes-closed balance task. Based on regression analyses, multiple clusters of voxels were identified showing a significant relationship between muscle spindle stimulation-induced neural activity and maximum center of pressure excursion in the anterior-posterior direction. In this case, increased activation was associated with greater balance performance in parietal, frontal, and insular cortical areas, as well as structures within the basal ganglia. These correlated regions were age- and foot-stimulation side-independent and largely localized to right-sided areas of the brain thought to be involved in monitoring stimulus-driven shifts of attention. These findings support the notion that, beyond fundamental peripheral reflex mechanisms, central processing of proprioceptive signals from the foot is critical for balance control.
Experimental Brain Research, 2004
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Neural Control of Balance During Walking
Frontiers in Physiology, 2018
Neural control of standing balance has been extensively studied. However, most falls occur during walking rather than standing, and findings from standing balance research do not necessarily carry over to walking. This is primarily due to the constraints of the gait cycle: Body configuration changes dramatically over the gait cycle, necessitating different responses as this configuration changes. Notably, certain responses can only be initiated at specific points in the gait cycle, leading to onset times ranging from 350 to 600 ms, much longer than what is observed during standing (50-200 ms). Here, we investigated the neural control of upright balance during walking. Specifically, how the brain transforms sensory information related to upright balance into corrective motor responses. We used visual disturbances of 20 healthy young subjects walking in a virtual reality cave to induce the perception of a fall to the side and analyzed the muscular responses, changes in ground reaction forces and body kinematics. Our results showed changes in swing leg foot placement and stance leg ankle roll that accelerate the body in the direction opposite of the visually induced fall stimulus, consistent with previous results. Surprisingly, ankle musculature activity changed rapidly in response to the stimulus, suggesting the presence of a direct reflexive pathway from the visual system to the spinal cord, similar to the vestibulospinal pathway. We also observed systematic modulation of the ankle push-off, indicating the discovery of a previously unobserved balance mechanism. Such modulation has implications not only for balance but plays a role in modulation of step width and length as well as cadence. These results indicated a temporally-coordinated series of balance responses over the gait cycle that insures flexible control of upright balance during walking.
Journal of Neurophysiology, 2013
Several studies have shown that the transmission of afferent inputs from the periphery to the somatosensory cortex is attenuated during the preparation of voluntary movements. In the present study, we tested whether sensory attenuation is also observed during the preparation of a voluntary step. It would appear dysfunctional to suppress somatosensory information, which is considered to be of the utmost importance for gait preparation. In this context, we predict that the somatosensory information is facilitated during gait preparation. To test this prediction, we recorded cortical somatosensory potentials (SEPs) evoked by bilateral lower limb vibration (i.e., proprioceptive inputs) during the preparation phase of a voluntary right-foot stepping movement (i.e., stepping condition). The subjects were also asked to remain still during and after the vibration as a control condition (i.e., static condition). The amplitude and timing of the early arrival of afferent inflow to the somatosensory cortices (i.e., P1-N1) were not significantly different between the static and stepping conditions. However, a large sustained negativity (i.e., late SEP) developed after the P1-N1 component, which was larger when subjects were preparing a step compared with standing. To determine whether this facilitation of proprioceptive inputs was related to gravitational equilibrium constraints, we performed the same experiment in microgravity. In the absence of equilibrium constraints, both the P1-N1 and late SEPs did not significantly differ between the static and stepping conditions. These observations provide neurophysiological evidence that the brain exerts a dynamic control over the transmission of the afferent signal according to their current relevance during movement preparation.
Feedforward neural control of toe walking in humans
The Journal of physiology, 2018
Toe walking requires careful control of the ankle muscles in order to absorb the impact of ground contact and maintain a stable position of the joint. The present study aimed to clarify the peripheral and central neural mechanisms involved. Fifteen healthy adults walked on a treadmill (3.0 km h). Tibialis Anterior (TA) and Soleus (Sol) EMG, knee and ankle joint angles and gastrocnemius-soleus muscle fascicle lengths were recorded. Peripheral and central contributions to the EMG activity were assessed by afferent blockade, H-reflex testing, Transcranial Magnetic Brain Stimulation (TMS) and sudden unloading of the planter flexor muscle-tendon complex. Sol EMG activity started prior to ground contact and remained high throughout stance. TA EMG activity, which is normally seen around ground contact during heel strike walking, was absent. Although stretch of the Achilles tendon-muscle complex was observed after ground contact, this was not associated with lengthening of the ankle plantar...
Cortical activation during executed, imagined, and observed foot movements
Neuroreport, 2008
Evidence suggests that executed, imagined, and observed movements share neural substrates, however, brain activation during the performance of these three tasks has not yet been examined during lower extremity movements. Functional MRI was performed in 10 healthy right-footed participants during imagined, executed, and observed right ankle movements. Task compliance was high, con¢rmed via behavioral assessment and electromyographic measurements. Each task was also associated with its own pro¢le of regional activation, however, overall, regional activation showed substantial overlap across the three lower extremity motor tasks. The ¢ndings suggest the utility of continued e¡orts to develop motor imagery and observation programs for improving lower extremity function in a range of clinical settings. NeuroReport19:625^630
PLoS ONE, 2012
The human locomotor system is flexible and enables humans to move without falling even under less than optimal conditions. Walking with high-heeled shoes constitutes an unstable condition and here we ask how the nervous system controls the ankle joint in this situation? We investigated the movement behavior of high-heeled and barefooted walking in eleven female subjects. The movement variability was quantified by calculation of approximate entropy (ApEn) in the ankle joint angle and the standard deviation (SD) of the stride time intervals. Electromyography (EMG) of the soleus (SO) and tibialis anterior (TA) muscles and the soleus Hoffmann (H-) reflex were measured at 4.0 km/h on a motor driven treadmill to reveal the underlying motor strategies in each walking condition. The ApEn of the ankle joint angle was significantly higher (p,0.01) during high-heeled (0.3860.08) than during barefooted walking (0.2860.07). During high-heeled walking, coactivation between the SO and TA muscles increased towards heel strike and the H-reflex was significantly increased in terminal swing by 40% (p,0.01). These observations show that high-heeled walking is characterized by a more complex and less predictable pattern than barefooted walking. Increased coactivation about the ankle joint together with increased excitability of the SO H-reflex in terminal swing phase indicates that the motor strategy was changed during high-heeled walking. Although, the participants were young, healthy and accustomed to high-heeled walking the results demonstrate that that walking on high-heels needs to be controlled differently from barefooted walking. We suggest that the higher variability reflects an adjusted neural strategy of the nervous system to control the ankle joint during high-heeled walking.
Cortical representation of rhythmic foot movements
Brain Research, 2008
The cortex is involved in rhythmic hand movements. The cortical contribution to rhythmic motor patterns of the feet, however, has never been evaluated in humans. In this study we investigated EEG activity related to rhythmic stepping and tapping movements in 10 healthy subjects. Subjects performed self-paced fast bilateral anti-phase, in-phase and unilateral rhythmic foot movements as well as an isometric cocontraction of the calf muscles, while being seated as relaxed as possible. Surface EMG from the anterior tibial muscles was recorded in parallel with a 64 channel EEG. Power spectra, corticomuscular coherence and corticomuscular delay were calculated. All subjects showed corticomuscular coherence at the stepping frequencies in the central midline region that extended further to the frontal mesial area. The magnitude and the topography of this coherence were equal for the right and left anterior tibial muscle and all movement conditions. During cocontraction there was coherence in the 15-30 Hz range which was refined to the central midline area. EEG-EMG delays were significant in 9 subjects with values between 14 and 26 ms, EMG-EEG feedback was only found in 6 subjects with delays between 25 and 40 ms. We conclude that rhythmic motor patterns of the feet are represented in the cortex, transmitted to the muscles with delays compatible with fast corticospinal transmission and fed back to the cortex. A similar cortical contribution may be important also for gait control in humans.
Cortical control of postural responses
Journal of Neural Transmission, 2007
This article reviews the evidence for cortical involvement in shaping postural responses evoked by external postural perturbations. Although responses to postural perturbations occur more quickly than the fastest voluntary movements, they have longer latencies than spinal stretch reflexes, suggesting greater potential for modification by the cortex. Postural responses include short, medium and long latency components of muscle activation with increasing involvement of the cerebral cortex as latencies increase. Evidence suggests that the cortex is also involved in changing postural responses with alterations in cognitive state, initial sensory-motor conditions, prior experience, and prior warning of a perturbation, all representing changes in "central set." Studies suggest that the cerebellar-cortical loop is responsible for adapting postural responses based on prior experience and the basal ganglia-cortical loop is responsible for pre-selecting and optimizing postural responses based on current context. Thus, the cerebral cortex likely influences longer latency postural responses both directly via corticospinal loops and shorter latency postural responses indirectly via communication with the brainstem centers that harbor the synergies for postural responses, thereby providing both speed and flexibility for preselecting and modifying environmentally appropriate responses to a loss of balance.
Large Postural Sways Prevent Foot Tactile Information From Fading: Neurophysiological Evidence
Cerebral Cortex Communications, 2020
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 ...
Brain Research, 2015
Right brain damage (RBD) following stroke often causes significant postural instability. In standing (without vision), patients with RBD are more unstable than those with left brain damage (LBD). We hypothesised that this postural instability would relate to the cortical integration of proprioceptive afferents. The aim of this study was to use tendon vibration to investigate whether these changes were specific to the paretic or non-paretic limbs. 14 LBD, 12 RBD patients and 20 healthy subjects were included. Displacement of the Centre of Pressure (CoP) was recorded during quiet standing, then during 3 vibration conditions (80 Hz-20 s): paretic limb, non-paretic limb (left and right limbs for control subjects) and bilateral. Vibration was applied separately to the peroneal and Achilles tendons. Mean antero-posterior position of the CoP, variability and velocity were calculated before (4 s), during and after (24 s) vibration. For all parameters, the strongest perturbation was during Achilles vibrations. The Achilles non-paretic condition induced a larger backward displacement than the Achilles paretic condition. This condition caused specific behaviour on the velocity: the LBD group was perturbed at the onset of the vibrations, but gradually recovered their stability; the RBD group was significantly perturbed thereafter. After bilateral Achilles vibration, RBD patients required the most time to restore initial posture. The reduction in use of information from the paretic limb may be a central strategy to deal with risk-of-fall situations such as during Achilles vibration. The postural behaviour is profoundly altered by lesions of the right hemisphere when proprioception is perturbed.
Modulation of proprioceptive inflow when initiating a step influences postural adjustments
Experimental Brain Research, 2010
A synergistic inclination of the whole body towards the supporting leg is required when producing a stepping movement. It serves to shift the centre of mass towards the stance foot. While the importance of sensory information in the setting of this postural adjustment is undisputed, it is currently unknown the extent to which proprioceptive aVerences (Ia) give rise to postural regulation during stepping movement when the availability of other sensory information relying on static linear acceleration (gravity) is no longer sensed in microgravity. We tested this possibility asking subjects to step forward with their eyes closed in normo-and microgravity environments. At the onset of the stepping movement, we vibrated the ankle muscles acting in the lateral direction to induce modiWcation of the aVerent inXow (Ia Wbres). Vibration-evoked movement (perceived movement) was in the same direction as the forthcoming body shift towards the supporting side (current movement). A control condition was performed without vibration. In both environments, when vibration was applied, the hip shift towards the supporting side decreased. These postural modiWcations occurred, however, earlier in normogravity before initiating the stepping movement than in microgravity (i.e. during the completion of the stepping movement). Our results suggest that proprioceptive information induced by vibration and aVerent inXow related to body movement exaggerated sense of movement. This biased perception led to the postural adjustment decrease. We propose that in both environments, proprioceptive inXow enables the subject to scale the postural adjustments, provided that body motion-induced aVerences are present to activate this postural control.
Direction-Dependent Control of Balance During Walking and Standing
Journal of Neurophysiology, 2009
We performed a whole-body mapping study of the effect of unilateral muscle vibration, eliciting spindle Ia firing, on the control of standing and walking in humans. During quiet stance, vibration applied to various muscles of the trunk-neck system and of the lower limb elicited a significant tilt in whole body postural orientation. The direction of vibration-induced postural tilt was consistent with a response compensatory for the illusory lengthening of the stimulated muscles. During walking, trunk-neck muscle vibration induced ample deviations of the locomotor trajectory toward the side opposite to the stimulation site. In contrast, no significant modifications of the locomotor trajectory could be detected when vibrating various muscles of the lower as well as upper limb. The absence of correlation between the effects of muscle vibration during walking and standing dismisses the possibility that vibration-induced postural changes can account for the observed deviations of the locomotor trajectory during walking. We conclude that the dissimilar effects of trunk-neck and lower limb muscle vibration during walking and standing reflect a general sensory-motor plan, whereby muscle Ia input is processed according to both the performed task and the body segment from which the sensory inflow arises.