Neural mechanisms influencing interlimb coordination during locomotion in humans: presynaptic modulation of forearm H-reflexes during leg cycling

Abstract

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.

Figure 1. Experimental set-up for leg cycling on the ergometer.

Nerve stimulation was delivered during cycling and static trials at the 12'clock position of the right pedal crank (thick lines of red). Green lightning bolt: median nerve stimulation (test stimulation for evoking the H-reflex). Blue lightning bolt: superficial radial nerve stimulation (conditioning stimulation to reduce Ia PSI and facilitate flexor carpi radialis (FCR) H-reflex amplitudes) Red lightning bolt: radial nerve stimulation (conditioning stimulation to increase Ia PSI and suppress FCR H-reflex amplitudes).

Figure 2. Effect of conditioning the flexor carpi radialis H-reflex with radial nerve stimulation during leg cycling and static activation.

(A) Typical averaged recordings of conditioned (black lines) and unconditioned (gray lines) H-reflex waveforms during static (upper traces) and cycling (lower traces) tasks obtained from a single subject. Grand means and SEM of magnitudes of the pre-stimulus EMG (B), H-reflex (C) and M-wave (D) during conditioned (black bars) and unconditioned (gray bars) trials. *p<0.01 significantly different from the unconditioned values for each task. +p<0.01 significantly different from the unconditioned static value.

Figure 3. Effect of conditioning the flexor carpi radialis H-reflex with superficial radial nerve stimulation during leg cycling and static activation obtained from 11 subjects.

Format and abbreviations as in Figure 2.

Figure 4. Effect of radial nerve conditioning on flexor carpi radialis (FCR) H-reflex amplitudes during leg cycling.

(A) Rectified and averaged FCR EMG and H-reflex waveforms following radial nerve stimulation [1.0× motor threshold (MT)] obtained from a single subject. Time zero on the x-axis is onset of conditioning stimulation. Please note that the EMG reflex responses (upper traces) had latencies that corresponded with the H-reflex (lower traces) during the conditioning-test interval. Horizontal arrows show analysis range for assessing ongoing FCR EMG. The arrow shows the suppressive response in the rectified EMG. (B) Conditioning effect of weak radial nerve stimulation (0.6×MT) on FCR H-reflex amplitude during static activation (gray traces) and leg cycling (black traces). (C) EMG responses following weak radial nerve stimulation (0.6×MT) during static and cycling tasks. Non-significant EMG responses were within 2 standard deviations (SD) of the pre-stimulus EMG levels. Broken lines in each panel represent a 2 SD band around the mean pre-stimulus EMG. Note that the stimulus artifact was replaced by the mean of the pre-stimulus EMG. Data in Figures 4A, B, and C were obtained from the same subject. (D) Grand means (± SEM) of H-reflex amplitudes (upper panel), M-waves (middle panel), and pre-stimulus EMG (lower panel) in the FCR muscle during radial nerve conditioning obtained from 9 subjects. * p<0.01 significantly different from the unconditioned values for each task. +p<0.01 significantly different from the unconditioned static value.

Figure 5. Effect of superficial radial nerve conditioning on flexor carpi radialis (FCR) H-reflex amplitudes during leg cycling.

(A) Rectified and averaged FCR EMG and H-reflex waveforms following superficial radial (SR) nerve stimulation [1.0× radiating threshold (RT)] obtained from a single subject. (B) Conditioning effect of FCR H-reflex with weak radial nerve stimulation (0.51×RT) during static and cycling tasks. (C) EMG responses following weak SR nerve stimulation (0.51×RT; just above perceptual threshold) during static activation and leg cycling. Please note that figures 5A, B, and C were obtained from same subject. (D) Grand means (± SEM) of H-reflexes (upper panel), M-waves (middle panel), and pre-stimulus EMG levels (lower panel) in the FCR muscle during SR nerve conditioning obtained from 9 subjects. * p<0.01 significantly different from the unconditioned values of each tasks. +p<0.01 significantly different from the unconditioned static values. Format and abbreviations as in Figure 4.

Figure 6. Schematic diagram outlining the possible neural pathways for integration of inputs arising from leg cycling and somatosensory conditioning stimulation on the presumed Ia presynaptic inhibitory pathway.

At the center is a simplified H-reflex pathway illustrating group Ia afferents synapsing with alpha motoneurons (MNs) of the flexor carpi radialis. Ia PSI and excitability of MNs are regulated by central commands and peripheral feedback related to leg cycling (black square). Inputs from the radial (red lightning bolt) and superficial radial nerves (blue lightning bolt) have excitatory and inhibitory connections onto Ia PSI interneurons (gray circle), respectively. The square with dashed line is a possible shared presynaptic pathways integrating locomotor-related inputs and somatosensory conditioning volleys during locomotion. Green lightning bolt: median nerve stimulation (test stimulation for evoking the FCR H-reflex).