Taryn Klarner

Neural Mechanisms Influencing Interlimb Coordination during Locomotion in Humans: Presynaptic Modulation of Forearm H-Reflexes during Leg Cycling

Presynaptic inhibition of transmission between Ia afferent terminals and alpha motoneurons (Ia PSI) is a major control mechanism associated with soleus H-reflex modulation during human locomotion. Rhythmic arm cycling suppresses soleus H-reflex amplitude by increasing segmental Ia PSI. There is a reciprocal organization in the human nervous system such that arm cycling modulates H-reflexes in leg muscles and leg cycling modulates H-reflexes in forearm muscles. However, comparatively little is known about mechanisms subserving the effects from leg to arm. Using a conditioning-test (C-T) stimulation paradigm, the purpose of this study was to test the hypothesis that changes in Ia PSI underlie the modulation of H-reflexes in forearm flexor muscles during leg cycling. Subjects performed leg cycling and static activation while H-reflexes were evoked in forearm flexor muscles. H-reflexes were conditioned with either electrical stimuli to the radial nerve (to increase Ia PSI; C-T interval  = 20 ms) or to the superficial radial (SR) nerve (to reduce Ia PSI; C-T interval  = 37–47 ms). While stationary, H-reflex amplitudes were significantly suppressed by radial nerve conditioning and facilitated by SR nerve conditioning. Leg cycling suppressed H-reflex amplitudes and the amount of this suppression was increased with radial nerve conditioning. SR conditioning stimulation removed the suppression of H-reflex amplitude resulting from leg cycling. Interestingly, these effects and interactions on H-reflex amplitudes were observed with subthreshold conditioning stimulus intensities (radial n., ∼0.6×MT; SR n., ∼ perceptual threshold) that did not have clear post synaptic effects. That is, did not evoke reflexes in the surface EMG of forearm flexor muscles. We conclude that the interaction between leg cycling and somatosensory conditioning of forearm H-reflex amplitudes is mediated by modulation of Ia PSI pathways. Overall our results support a conservation of neural control mechanisms between the arms and legs during locomotor behaviors in humans.

Neuromechanical interactions between the limbs during human locomotion: an evolutionary perspective with translation to rehabilitation.

During bipedal locomotor activities, humans use elements of quadrupedal neuronal limb control. Evolutionary constraints can help inform the historical ancestry for preservation of these core control elements support transfer of the huge body of quadrupedal non-human animal literature to human rehabilitation. In particular, this has translational applications for neurological rehabilitation after neurotrauma where interlimb coordination is lost or compromised. The present state of the field supports including arm activity in addition to leg activity as a component of gait retraining after neurotrauma.

Cutaneous stimulation of discrete regions of the sole during locomotion produces “sensory steering” of the foot

BackgroundWhile the neural and mechanical effects of whole nerve cutaneous stimulation on human locomotion have been previously studied, there is less information about effects evoked by activation of discrete skin regions on the sole of the foot. Electrical stimulation of discrete foot regions evokes position-modulated patterns of cutaneous reflexes in muscles acting at the ankle during standing but data during walking are lacking. Here, non-noxious electrical stimulation was delivered to five discrete locations on the sole of the foot (heel, and medial and lateral sites on the midfoot and forefoot) during treadmill walking. EMG activity from muscles acting at the hip, knee and ankle were recorded along with movement at these three joints. Additionally, 3 force sensing resistors measuring continuous force changes were placed at the heel, and the medial and lateral aspects of the right foot sole. All data were sorted based on stimulus occurrence in twelve step-cycle phases, before being averaged together within a phase for subsequent analysis.MethodsNon-noxious electrical stimulation was delivered to five discrete locations on the sole of the foot (heel, and medial and lateral sites on the midfoot and forefoot) during treadmill walking. EMG activity from muscles acting at the hip, knee and ankle were recorded along with movement at these three joints. Additionally, 3 force sensing resistors measuring continuous force changes were placed at the heel, and the medial and lateral aspects of the right foot sole. All data were sorted based on stimulus occurrence in twelve step-cycle phases, before being averaged together within a phase for subsequent analysis.ResultsThe results demonstrate statistically significant dynamic changes in reflex amplitudes, kinematics and foot sole pressures that are site-specific and phase-dependent. The general trends demonstrate responses producing decreased underfoot pressure at the site of stimulation.ConclusionsThe responses to stimulation of discrete locations on the foot sole evoke a kind of “sensory steering” that may promote balance and maintenance of locomotion through the modulation of limb loading and foot placement. These results have implications for using sensory stimulation as a therapeutic modality during gait retraining (e.g. after stroke) as well as for footwear design and implementation of foot sole contact surfaces during gait.

Preservation of common rhythmic locomotor control despite weakened supraspinal regulation after stroke.

The basic pattern of arm and leg movement during rhythmic locomotor tasks is supported by common central neural control from spinal and supraspinal centers in neurologically intact participants. The purpose of this study was to test the hypothesis that following a cerebrovascular accident, shared systems from interlimb cutaneous networks facilitating arm and leg coordination persist across locomotor tasks. Twelve stroke participants (>6 months post CVA) performed arm and leg (A&L) cycling using a stationary ergometer and walking on a motorized treadmill. In both tasks cutaneous reflexes were evoked via surface stimulation of the nerves innervating the dorsum of the hand (superficial radial; SR) and foot (superficial peroneal; SP) of the less affected limbs. Electromyographic (EMG) activity from the tibialis anterior, soleus, flexor carpi radialis, and posterior deltoid were recorded bilaterally with surface electrodes. Full-wave rectified and filtered EMG data were separated into eight equal parts or phases and aligned to begin with maximum knee extension for both walking and A&L cycling. At each phase of movement, background EMG data were quantified as the peak normalized response for each participant and cutaneous reflexes were quantified as the average cumulative reflex over 150 ms following stimulation. In general, background EMG was similar between walking and A&L cycling, seen especially in the distal leg muscles. Cutaneous reflexes were evident and modified in the less and more affected limbs during walking and A&L cycling and similar modulation patterns were observed suggesting activity in related control networks between tasks. After a stroke common neural patterning from conserved subcortical regulation is seen supporting the notion of a common core in locomotor tasks involving arm and leg movement. This has translational implications for rehabilitation where A&L cycling could be usefully applied to improve walking function.

Exploiting Interlimb Arm and Leg Connections for Walking Rehabilitation: A Training Intervention in Stroke

Rhythmic arm and leg (A&L) movements share common elements of neural control. The extent to which A&L cycling training can lead to training adaptations which transfer to improved walking function remains untested. The purpose of this study was to test the efficacy of A&L cycling training as a modality to improve locomotor function after stroke. Nineteen chronic stroke (>six months) participants were recruited and performed 30 minutes of A&L cycling training three times a week for five weeks. Changes in walking function were assessed with (1) clinical tests; (2) strength during isometric contractions; and (3) treadmill walking performance and cutaneous reflex modulation. A multiple baseline (3 pretests) within-subject control design was used. Data show that A&L cycling training improved clinical walking status increased strength by ~25%, improved modulation of muscle activity by ~25%, increased range of motion by ~20%, decreased stride duration, increased frequency, and improved modulation of cutaneous reflexes during treadmill walking. On most variables, the majority of participants showed a significant improvement in walking ability. These results suggest that exploiting arm and leg connections with A&L cycling training, an accessible and cost-effective training modality, could be used to improve walking ability after stroke.

Long-Term Plasticity in Reflex Excitability Induced by Five Weeks of Arm and Leg Cycling Training after Stroke

Neural connections remain partially viable after stroke, and access to these residual connections provides a substrate for training-induced plasticity. The objective of this project was to test if reflex excitability could be modified with arm and leg (A & L) cycling training. Nineteen individuals with chronic stroke (more than six months postlesion) performed 30 min of A & L cycling training three times a week for five weeks. Changes in reflex excitability were inferred from modulation of cutaneous and stretch reflexes. A multiple baseline (three pretests) within-subject control design was used. Plasticity in reflex excitability was determined as an increase in the conditioning effect of arm cycling on soleus stretch reflex amplitude on the more affected side, by the index of modulation, and by the modulation ratio between sides for cutaneous reflexes. In general, A & L cycling training induces plasticity and modifies reflex excitability after stroke.

Regionally distinct cutaneous afferent populations contribute to reflex modulation evoked by stimulation of the tibial nerve during walking

During walking, cutaneous reflexes in ankle flexor muscle [tibialis anterior (TA)] evoked by tibial nerve (TIB) stimulation are predominantly facilitatory at early swing phase but reverse to suppression at late swing phase. Although the TIB innervates a large portion of the skin of the foot sole, the extent to which specific foot-sole regions contribute to the reflex reversals during walking remains unclear. Therefore, we investigated regional cutaneous contributions from discrete portions of the foot sole on reflex reversal in TA following TIB stimulation during walking. Summation effects on reflex amplitudes, when applying combined stimulation from foot-sole regions with TIB, were examined. Middle latency responses (MLRs; 70-120 ms) after TIB stimulation were strongly facilitated during the late stance to mid-swing phases and reversed to suppression just before heel (HL) strike. Both forefoot-medial (f-M) and forefoot-lateral stimulation in the foot sole induced facilitation during stance-to-swing transition phases, but HL stimulation evoked suppression during the late stance to the end of swing phases. At the stance-to-swing transition, a summation of MLR amplitude occurred only for combined f-M&TIB stimulation. However, the same was not true for the combined HL&TIB stimulation. At the swing-to-stance transition, there was a suppressive reflex summation only for HL&TIB stimulation. In contrast, this summation was not observed for the f-M&TIB stimulation. Our results suggest that reflex reversals evoked by TIB stimulation arise from distinct reflex pathways to TA produced by separate afferent populations innervating specific regions of the foot sole.

Beyond the Bottom of the Foot: Topographic Organization of the Foot Dorsum in Walking

Introduction Sensory feedback from the foot dorsum during walking has only been studied globally by whole nerve stimulation. Stimulating the main nerve innervating the dorsal surface produces a functional stumble corrective response that is phase-dependently modulated. We speculated that effects evoked by activation of discrete skin regions on the foot dorsum would be topographically organized, as with the foot sole. Methods Nonnoxious electrical stimulation was delivered to five discrete locations on the dorsal surface of the foot during treadmill walking. Muscle activity from muscles acting at the ankle, knee, hip, and shoulder were recorded along with ankle, knee, and hip kinematics and kinetic information from forces under the foot. All data were sorted on the basis of stimulus occurrence in 12 step cycle phases, before being averaged together within a phase for subsequent analysis. Results Results reveal dynamic changes in reflex amplitudes and kinematics that are site specific and phase dependent. Most responses from discrete sites on the foot dorsum were seen in the swing phase suggesting function to conform foot trajectory to maintain stability of the moving limb. In general, responses from lateral stimulation differed from medial stimulation, and effects were largest from stimulation at the distal end of the foot at the metatarsals; that is, in anatomical locations where actual impact with an object in the environment is most likely during swing. Responses to stimulation extend to include muscles at the hip and shoulder. Conclusions We reveal that afferent feedback from specific cutaneous locations on the foot dorsum influences stance and swing phase corrective responses. This emphasizes the critical importance of feedback from the entire foot surface in locomotor control and has application for rehabilitation after neurological injury and in footwear development.

Equivalent Bilateral Early Latency Cutaneous Reflex Amplitudes during Graded Contractions in Right Handers

Functional asymmetries exist in right handers due to asymmetries at multiple levels of the nervous system. Spinally-mediated contributions have been assessed using the Hoffmann reflex but have provided varying results. The purpose of this paper was to explore possible spinally-mediated contributions from cutaneous receptors to the asymmetry in strength seen in right handed individuals. Asymmetries were assessed by maximal voluntary contraction force during wrist flexion, extension, and handgrip. Peak muscle activation (EMGmax) was measured in the flexor (FCR) and extensor (ECR) carpi radialis and normalized to the maximal evoked motor responses (M-Max) elicited via median (MED) or radial nerve stimulation applied proximal to the elbow joint. Cutaneous reflexes were evoked by trains of stimulation (5x1ms @ 300Hz) delivered to the superficial radial (SR) or MED at the wrist during graded ipsilateral wrist extension contractions of 5, 10, 25, and 50% EMGmax. Results indicate that asymmetries exist for both strength and maximal muscle activation normalized to M-Max. Early latency (50 – 70 ms) cutaneous reflex amplitudes are larger on the dominant (right) side. However, when normalized to background EMG these differences disappear. Thus, when considering the same relative input, cutaneous afferent pathways have similar bilateral effects during ongoing muscle activity.

Neuromechanical Interlimb Interactions and Rehabilitation of Walking after Stroke

Bipedal humans operate using elements of quadrupedal neuronal limb control during locomotion. This has significant implications for supporting transfer of the huge body of quadrupedal animal literature to human rehabilitation. In particular, this has translational applications for neurological rehabilitation after stroke where interlimb coordination is compromised. The data supports including arm activity in addition to leg activity as a component of gait retraining after stroke. An additional component is to consider strength training of the less affected limb to improve motor output of the more affected limb when that limb is too weak to be initially incorporated in functional rehabilitation. The major concept is to use activity related to the less affected limbs to modulate output of the more affected limbs after stroke. A key example is to incorporate arm activity into rehabilitation of leg motion in stepping after stroke.