Catherine R. Lowrey

Feedback control during voluntary motor actions

Humans possess an impressive ability to generate goal-oriented motor actions to move and interact with the environment. The planning and initiation of these body movements is supported by highly distributed cortical and subcortical circuits. Recent studies, inspired by advanced control theory, highlight similar sophistication when we make online corrections to counter small disturbances of the limb or altered visual feedback. Such goal-directed feedback is likely generated by the same neural circuits associated with motor planning and initiation. These common neural substrates afford a highly responsive system to maintain goal-directed control and rapidly select new motor actions as required to deftly move and interact in a complex world.

Skin sensory information from the dorsum of the foot and ankle is necessary for kinesthesia at the ankle joint

Previous research has shown that skin is capable of providing kinesthetic cues at particular joints but we are unsure how these cues are used by the central nervous system. The current study attempted to identify the role of skin on the dorsum of the ankle during a joint matching task. A 30cm patch of skin was anesthetized and matching accuracy in a passive joint matching task was compared before and after skin anesthetization. Goniometers were used to measure ankle angular displacement. Four target angles were used in the matching task, 7° of dorsiflexion, 7°, 14° and 21° of plantarflexion. We hypothesized that, based on the location of skin anesthetized, only the plantarflexion matching tasks would be affected. Absolute error (accuracy) increased significantly for all angles when the skin was anesthetized. Directional error indicated that overall subjects tended to undershoot the target angles, significantly more so for 21° of plantarflexion when the skin was anesthetized. Following anesthetization, variable error (measure of task difficulty) increased significantly at 7° of dorsiflexion and 21° of plantarflexion. These results indicate that the subjects were less accurate and more variable when skin sensation was reduced suggesting that skin information plays an important role in kinesthesia at the ankle.

A Novel Robotic Task for Assessing Impairments in Bimanual Coordination Post-Stroke

Background: Bimanual tasks are integral to the performance of many activities of daily living, but impairments in bimanual coordination following stroke are not well quantified with existing clinical tools. Objective: The current study outlines a novel robotic task for the objective and quantitative assessment of bimanual impairment following stroke. Methods: We developed a robotic, bimanual assessment task using the KINARM robot. The task involved moving a virtual ball on a bar linking the two hands, to targets displayed using a virtual reality system. Seventy-five healthy control participants and 23 participants with sub-acute stroke were assessed using the task. Task performance of participants with stroke was compared with the healthy control group, as well as to standard clinical tests (Chedoke- McMaster Stroke Assessment (CMSA) arm and hand, Functional Independence Measure (FIM), Montreal Cognitive Assessment (MoCA) and Behavioural Inattention Test (BIT)). Results: A range of impairments in bimanual task performance was found for participants with stroke. As a group, 85% of participants with stroke had impairments on more task parameters than 95% of healthy controls. Participants with stroke commonly displayed impairments in task success (fewer targets hit); movement metrics (slower movement speed) and bimanual coordination (larger difference in reaction time between hands, greater number of speed peaks with unaffected versus affected limb and greater absolute tilt of the bar). Overall performance of the robotic task (total number of parameters ‘failed’) was significantly correlated with motor performance scores (CMSA, r=-0.6) and strongly correlated with measures of functional ability (FIM motor, r=-0.8). Conclusions: A robotic bimanual task can identify impairments in a population of stroke participants and provides a quantitative measure of bimanual coordination.

Selective skin sensitivity changes and sensory reweighting following short-duration space flight

Skin sensory input from the foot soles is coupled with vestibular input to facilitate body orientation in a gravitational environment. Anecdotal observations suggest that foot sole skin becomes hypersensitive following space flight. The veritable level of skin sensitivity and its impact on postural disequilibrium observed post space flight have not been documented. Skin sensitivity of astronauts (n = 11) was measured as vibration perception at the great toe, fifth metatarsal and heel. Frequencies targeted four classes of receptors: 3 and 25 Hz for slow-adapting (SA) receptors and 60 and 250 Hz for fast-adapting (FA) receptors. Data were collected pre- and post-space flight. We hypothesized that skin sensitivity would increase post-space flight and correlate to balance measures. Decreased skin sensitivity was found on landing day at 3 and 25 Hz on the great toe. Hypersensitivity was found for a subset of astronauts (n = 6) with significantly increased sensitivity to 250 Hz at the heel. This subset displayed a greater reduction in computerized dynamic posturography (CDP) equilibrium (EQ) scores (-54%) on landing vs. non-hypersensitive participants (-11%). Observed hyposensitivity of SA (pressure) receptors may indicate a strategy to reduce pressure input during periods of unloading. Hypersensitivity of FAs coupled with reduced EQ scores may reflect targeted sensory reweighting. Altered gravito-inertial environments reduce vestibular function in balance control which may trigger increased weighting of FAs (that signal foot contact, slips). Understanding modulations to skin sensitivity has translational implications for mitigating postural disequilibrium following space flight and for on-Earth preventative strategies for imbalance in older adults.

Single low-threshold afferents innervating the skin of the human foot modulate ongoing muscle activity in the upper limbs

We have shown for the first time that single cutaneous afferents in the foot dorsum have significant reflex coupling to motoneurons supplying muscles in the upper limb, particularly posterior deltoid and triceps brachii. These observations strengthen what we know from whole nerve stimulation, that skin on the foot and ankle can contribute to the modulation of interlimb muscles in distant innervation territories. The current work provides evidence of the mechanism behind the reflex, where one single skin afferent can evoke a reflex response, rather than a population. Nineteen of forty-one (46%) single cutaneous afferents isolated in the dorsum or plantar surface of the foot elicited a significant modulation of muscle activity in the upper limb. Identification of single afferents in this reflex indicates the strength of the connection and, ultimately, the importance of foot skin in interlimb coordination. The median response magnitude was 2.29% of background EMG, and the size of the evoked response did not significantly differ among the four mechanoreceptor classes (P > 0.1). Interestingly, although the distribution of afferents types did not differ across the foot dorsum, there was a significantly greater coupling response from receptors located on the medial aspect of the foot dorsum (P < 0.01). Furthermore, the most consistent coupling with upper limb muscles was demonstrated by type I afferents (fast and slowly adapting). This work contributes to the current literature on receptor specificity, supporting the view that individual classes of cutaneous afferents may subserve specific roles in kinesthesia, reflexes, and tactile perception.

Modulation of the soleus H-reflex following galvanic vestibular stimulation and cutaneous stimulation in prone human subjects

There is evidence to suggest that vestibular and somatosensory inputs may interact when they are processed by the central nervous system, although the nature of the individual sensory contributions to this interaction is unknown. We examined the effects of a combined vestibular and cutaneous conditioning stimulus on the motoneuron pool that supplies the soleus muscle via the Hoffman reflex (H‐reflex). We applied galvanic vestibular stimulation (GVS; bipolar, binaural, 500 ms, 2.5‐mA square‐wave pulse) and cutaneous stimulation (medial plantar nerve; 11 ms, three‐pulse train, 200 HZ) to prone human subjects and examined changes in the amplitude of the H‐reflex. GVS alone caused facilitation (approximately 20%) of the H‐reflex, whereas ipsilateral cutaneous stimulation alone caused a 26% inhibition. Paired GVS and cutaneous stimulation resulted in a linear summation of the individual conditioning effects. H‐reflex amplitudes observed after paired conditioning with GVS and cutaneous stimulation could be predicted from the amplitudes observed with individual conditioning. These results suggest that in the prone position, when the muscles are not posturally engaged, vestibular and somatosensory information appear to sum in a linear fashion to influence the reflex response of lower limb motoneurons. Muscle Nerve 40: 213–220, 2009

Rapid and flexible whole body postural responses are evoked from perturbations to the upper limb during goal-directed reaching

An important aspect of motor control is the ability to perform tasks with the upper limbs while maintaining whole body balance. However, little is known about the coordination of upper limb voluntary and whole body postural control after mechanical disturbances that require both upper limb motor corrections to attain a behavioral goal and lower limb motor responses to maintain whole body balance. The present study identified the temporal organization of muscle responses and center of pressure (COP) changes following mechanical perturbations during reaching. Our results demonstrate that muscle responses in the upper limb are evoked first (∼50 ms), with lower limb muscle activity occurring immediately after, in as little as ∼60 ms after perturbation. Hand motion was immediately altered by the load, while COP changes occurred after ∼100 ms, when lower limb muscle activity was already present. Our secondary findings showed that both muscle activity and COP changes were influenced by behavioral context (by altering target shape, circle vs. rectangle). Voluntary and postural actions initially directed the hand toward the center of both target types, but after the perturbation upper limb and postural responses redirected the hand toward different spatial locations along the rectangle. Muscle activity was increased for both upper and lower limbs when correcting to the circle vs. the rectangle, and these differences emerged as early as the long-latency epoch (∼75-120 ms). Our results demonstrate that postural responses are rapidly and flexibly altered to consider the behavioral goal of the upper limb.NEW & NOTEWORTHY The present work establishes that, when reaching to a target while standing, perturbations applied to the upper limb elicit a rapid response in lower limb muscles. Unlike voluntary movements, postural responses do not occur before corrections of the upper limb. We show the first evidence that corrective postural adjustments are modulated by upper limb behavioral context (target shape). Importantly, this indicates that postural responses take into account upper limb feedback for online control.

Selective weighting of cutaneous receptor feedback and associated balance impairments following short duration space flight

The present study investigated the perception of low frequency (3 Hz) vibration on the foot sole and its relationship to standing balance following short duration space flight in nine astronauts. Both 3 Hz vibration perception threshold (VPT) and standing balance measures increased on landing day compared to pre-flight. Contrary to our hypothesis, a positive linear relationship between these measures was not observed; however astronauts with the most sensitive skin (lowest 3 Hz VPT) were found to have the largest sway on landing day. While the change in foot sole sensitivity does not appear to directly relate to standing balance control, an exploratory strategy may be employed by astronauts whose threshold to pressure information is lower. Understanding sensory adaptations and balance control has implications to improve balance control strategies following space flight and in sensory impaired populations on earth.