Intralimb and Interlimb Cutaneous Reflexes during Locomotion in the Intact Cat

Abstract

When the foot contacts an obstacle during locomotion, cutaneous inputs activate spinal circuits to ensure dynamic balance and forward progression. In quadrupeds, this requires coordinated reflex responses between the four limbs. Here, we investigated the patterns and phasic modulation of cutaneous reflexes in forelimb and hindlimb muscles evoked by inputs from all four limbs. Five female cats were implanted to record muscle activity and to stimulate the superficial peroneal and superficial radial nerves during locomotion. Stimulating these nerves evoked short-, mid-, and longer-latency excitatory and/or inhibitory responses in all four limbs that were phase-dependent. The largest responses were generally observed during the peak activity of the muscle. Cutaneous reflexes during mid-swing were consistent with flexion of the homonymous limb and accompanied by modification of the stance phases of the other three limbs, by coactivating flexors and extensors and/or by delaying push-off. Cutaneous reflexes during mid-stance were consistent with stabilizing the homonymous limb by delaying and then facilitating its push-off and modifying the support phases of the homolateral and diagonal limbs, characterized by coactivating flexors and extensors, reinforcing extensor activity and/or delaying push-off. The shortest latencies of homolateral and diagonal responses were consistent with fast-conducting disynaptic or trisynaptic pathways. Descending homolateral and diagonal pathways from the forelimbs to the hindlimbs had a higher probability of eliciting responses compared with ascending pathways from the hindlimbs to the forelimbs. Thus, in quadrupeds, intralimb and interlimb reflexes activated by cutaneous inputs ensure dynamic coordination of the four limbs, producing a whole-body response. The skin contains receptors that, when activated, send inputs to spinal circuits, signaling a perturbation. Rapid responses, or reflexes, in muscles of the contacted limb and opposite homologous limb help maintain balance and forward progression. Here, we investigated reflexes during quadrupedal locomotion in the cat by electrically stimulating cutaneous nerves in each of the four limbs. Functionally, responses appear to modify the trajectory or stabilize the movement of the stimulated limb while modifying the support phase of the other limbs. Reflexes between limbs are mediated by fast-conducting pathways that involve excitatory and inhibitory circuits controlling each limb. The comparatively stronger descending pathways from cervical to lumbar circuits controlling the forelimbs and hindlimbs, respectively, could serve a protective function.

On the organization of the locomotor CPG: insights from split-belt locomotion and mathematical modeling

“…Therefore, our study provides additional support for the important role of V3 CINs and the existence of inhibitory commissural pathways from extensor half-centers to contralateral flexor half-centers, mediated by V3 and (presumably) V1 interneurons (Danner et al, 2019). Although this prediction still awaits experimental testing, crossed inhibition to flexors (by afferent stimulation) has been observed in anesthetized preparations (Jankowska et al, 2005;Jankowska & Edgley, 2010) and during locomotion in intact cats (Hurteau et al, 2018) as well as in mouse (Laflamme & Akay, 2018) and…”

“…Before and after experiments, cats were housed and fed in a dedicated room within the animal care facility of the Faculty of Medicine and Health Sciences at the Université de Sherbrooke. As part of our effort to maximize the scientific output of each animal, 10 of 11 animals were used in other studies to answer different scientific questions (Frigon et al, 2013;Thibaudier et al, 2013;D'Angelo et al, 2014;Frigon et al, 2014;Thibaudier & Frigon, 2014;Dambreville et al, 2015;Frigon et al, 2015;Hurteau et al, 2015;Dambreville et al, 2016;Frigon et al, 2017;Hurteau et al, 2017;Kuczynski et al, 2017;Thibaudier et al, 2017;Harnie et al, 2018;Hurteau & Frigon, 2018;Hurteau et al, 2018;Desrochers et al, 2019). The experimental studies complied with the ARRIVE guidelines (Kilkenny et al, 2010) and principles of animal research established by the Journal of Physiology (Grundy, 2015).…”

Spinal control of muscle synergies for adult mammalian locomotion

“…We implanted electrodes to record hindlimb muscle activity (EMG, electromyography) in intact cats under aseptic conditions in an operating room with sterilized equipment, as described previously (Hurteau et al . , ; Frigon et al . ).…”

“…We implanted electrodes to record hindlimb muscle activity (EMG, electromyography) in intact cats under aseptic conditions in an operating room with sterilized equipment, as described previously (Hurteau et al , 2018Frigon et al 2015). Before surgery, induction was made with an intramuscular injection of Butorphanol (0.4 mg kg −1 ), Acepromazine (0.1 mg kg −1 ), Glycopyrrolate (0.01 mg kg −1 ) and ketamine/diazepam (0.11 ml kg −1 in a 1:1 ratio).…”

On the Organization of the Locomotor CPG: Insights From Split-Belt Locomotion and Mathematical Modeling

“…Before and after experiments, cats were housed and fed in a dedicated room within the animal care facility of the Faculty of Medicine and Health Sciences at the Université de Sherbrooke. As part of our effort to maximize the scientific output of each animal, 10 of 11 animals were used in other studies to answer different scientific questions ( Frigon et al, 2013 , 2014 , 2015 , 2017 ; Thibaudier et al, 2013 , 2017 ; D’Angelo et al, 2014 ; Thibaudier and Frigon, 2014 ; Dambreville et al, 2015 , 2016 ; Hurteau et al, 2015 , 2017 , 2018 ; Kuczynski et al, 2017 ; Harnie et al, 2018 ; Hurteau and Frigon, 2018 ; Desrochers et al, 2019 ). The experimental studies complied with the ARRIVE guidelines ( Kilkenny et al, 2010 ) and principles of animal research established by the Journal of Physiology ( Grundy, 2015 ).…”