A sensory signal related to left-right symmetry modulates intra- and interlimb cutaneous reflexes during locomotion in intact cats

Abstract

IntroductionDuring locomotion, cutaneous reflexes play an essential role in rapidly responding to an external perturbation, for example, to prevent a fall when the foot contacts an obstacle. In cats and humans, cutaneous reflexes involve all four limbs and are task- and phase modulated to generate functionally appropriate whole-body responses.MethodsTo assess task-dependent modulation of cutaneous interlimb reflexes, we electrically stimulated the superficial radial or superficial peroneal nerves in adult cats and recorded muscle activity in the four limbs during tied-belt (equal left-right speeds) and split-belt (different left-right speeds) locomotion.ResultsWe show that the pattern of intra- and interlimb cutaneous reflexes in fore- and hindlimbs muscles and their phase-dependent modulation were conserved during tied-belt and split-belt locomotion. Short-latency cutaneous reflex responses to muscles of the stimulated limb were more likely to be evoked and phase-modulated when compared to muscles in the other limbs. In some muscles, the degree of reflex modulation was significantly reduced during split-belt locomotion compared to tied-belt conditions. Split-belt locomotion increased the step-by-step variability of left-right symmetry, particularly spatially.DiscussionThese results suggest that sensory signals related to left-right symmetry reduce cutaneous reflex modulation, potentially to avoid destabilizing an unstable pattern.

Changes in intra‐ and interlimb reflexes from hindlimb cutaneous afferents after staggered thoracic lateral hemisections during locomotion in cats

“…The investigators understand the ethical principles under which the journal operates and our work complies with this animal ethics checklist. In order to maximize the scientific output of each animal, they were used in other studies to investigate different scientific questions, some of which have been published (Audet et al, 2023;Lecomte et al, 2022Lecomte et al, , 2023Mari et al, 2023;Merlet et al, 2022).…”

“…This value was then divided by the baseline C occurring in the same time window giving N1 and P3 normalized amplitudes for the left soleus. [Colour figure can be viewed at wileyonlinelibrary.com] & Stein, 1978;Hurteau et al, 2017Loeb, 1993;Mari et al, 2023;Pratt et al, 1991) with 97.5% confidence intervals. We measured the latencies of responses from stimulation onset to response onset.…”

“…For example, cats have varying levels of physical activity after spinal lesions, with some more active than others. Before and after staggered hemisections, cats performed a variety of treadmill and walkway tasks to answer other scientific questions (Audet et al, 2023;Lecomte et al, 2022Lecomte et al, , 2023Mari et al, 2023;Merlet et al, 2022). We believe that these tasks standardized the level of physical activity across animals, providing a minimal baseline.…”

“…In humans, interlimb reflexes evoked in arm muscles with electrical stimulation of the tibial nerves at rest, were strengthened following cervical SCI (Calancie et al., 2002). We know that interlimb reflexes evoked by stimulating cutaneous nerves of the fore‐ and hindlimbs are modulated during locomotion in cats and humans (Haridas & Zehr, 2003; Hurteau et al., 2018; Mari et al., 2023; Merlet et al., 2022), likely contributing to limb coordination, but we do not know how they change following SCI and if their loss could explain impairments in limb coordination during locomotion.…”

“…In the present study, we electrically stimulated the superficial peroneal nerve (SP) that innervates the foot dorsum, responsible for the stumbling corrective reaction in cats and humans (Duysens & Loeb, 1980; Forssberg, 1979; Forssberg et al., 1977; Prochazka et al., 1978; Quevedo et al., 2005a, b; Schillings et al., 1996; Van Wezel et al., 1997; Wand et al., 1980; Zehr et al., 1997), during treadmill locomotion. In cats, stimulating the SP nerve elicits short‐ (7–18 ms), mid‐ (19–34 ms) and long‐latency (35–60 ms) responses in all four limbs (Hurteau et al., 2018; Mari et al., 2023; Merlet et al., 2022). Mid‐ and long‐latency responses are thought to involve supraspinal contributions (Frigon & Rossignol, 2008; Fuwa et al., 1991; Hurteau & Frigon, 2018; LaBella et al., 1992).…”