Nonlinear Modulation of Cutaneous Reflexes with Increasing Speed of Locomotion in Spinal Cats

Abstract

Cutaneous reflexes are important for responding rapidly to perturbations, correcting limb trajectory, and strengthening support. During locomotion, they are modulated by phase to generate functionally appropriate responses. The goal of the present study was to determine whether cutaneous reflexes and their phase-dependent modulation are altered with increasing speed and if this is accomplished at the spinal level. Four adult cats that recovered stable hindlimb locomotion after spinal transection were implanted with electrodes to record hindlimb muscle activity chronically and to stimulate the superficial peroneal nerve electrically to evoke cutaneous reflexes. The speed-dependent modulation of cutaneous reflexes was assessed by evoking and characterizing ipsilateral and contralateral responses in semitendinosus, vastus lateralis, and lateral gastrocnemius muscles at four treadmill speeds: 0.2, 0.4, 0.6, and 0.8 m/s. The amplitudes of ipsilateral and contralateral responses were largest at intermediate speeds of 0.4 and 0.6 m/s, followed by the slowest and fastest speeds of 0.2 and 0.8 m/s, respectively. The phase-dependent modulation of reflexes was maintained across speeds, with ipsilateral and contralateral responses peaking during the stance-to-swing transition and swing phase of the ipsilateral limb or midstance of the contralateral limb. Reflex modulation across speeds also correlated with the spatial symmetry of the locomotor pattern, but not with temporal symmetry. That the cutaneous reflex amplitude in all muscles was similarly modulated with increasing speed independently of the background level of muscle activity is consistent with a generalized premotoneuronal spinal control mechanism that could help to stabilize the locomotor pattern when changing speed. When walking, receptors located in the skin respond to mechanical pressure and send signals to the CNS to correct the trajectory of the limb and to reinforce weight support. These signals produce different responses, or reflexes, if they occur when the foot is contacting the ground or in the air. This is known as phase-dependent modulation of reflexes. However, when walking at faster speeds, we do not know if and how these reflexes are changed. In the present study, we show that reflexes from the skin are modulated with speed and that this is controlled at the level of the spinal cord. This modulation could be important in preventing sensory signals from destabilizing the walking pattern.

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 . ).…”

A Spinal Mechanism Related to Left–Right Symmetry Reduces Cutaneous Reflex Modulation Independently of Speed During Split-Belt Locomotion

“…For the spatial phasing index, we first measured stride length as the horizontal distance traveled from stance offset to onset plus the distance traveled by the opposite treadmill belt during the swing phase, which corresponds to swing duration multiplied by treadmill speed (Fig. 1B) (Goetz et al, 2012;Thibaudier and Frigon, 2014;Harnie et al, 2018). We then measured step length as the distance between the leading and trailing limb at stance onset of the leading limb (Hoogkamer et al, 2014).…”

“…Stepping on a split-belt treadmill also simulates a limping gait (Duysens et al, 2004(Duysens et al, , 2012Mc-Fadyen et al, 2009;Hoogkamer et al, 2015), particularly in cats, in which the pattern does not adapt to prolonged exposure (Kuczynski et al, 2017), contrary to humans (Prokop et al, 1995;Reisman et al, 2005). We consider the limping gait induced by split-belt locomotion an unstable form of locomotion, as observed in some pathologies (Harris-Love et al, 2001;Duysens et al, 2012;Handžić and Reed, 2015). Here, we define stability as the body's resistance to disruption of dynamic balance (equilibrium).…”

“…The stumbling corrective reaction, or cutaneous reflexes consistent with it, is present in the hindlimbs of cats with a complete spinal transection (spinal cats), indicating that it is organized within the spinal cord (Forssberg et al, 1975(Forssberg et al, , 1977 Frigon and Rossignol, 2008a;Hurteau et al, 2017). Moreover, in cats and humans, reflexes evoked by stimulating the superficial peroneal (SP) nerve, which supplies the skin of the foot dorsum, are observed in the four limbs, indicating that the stumbling corrective reaction is a whole-body response (Haridas and Zehr, 2003;Haridas et al, 2006;Hurteau et al, 2018).…”

Lack of adaptation during prolonged split‐belt locomotion in the intact and spinal cat

“…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 reduce the number of animals that we use in research, all cats participated in other studies to address different scientific questions Thibaudier et al 2013Thibaudier et al , 2017D'Angelo et al 2014;Dambreville et al 2015Dambreville et al , 2016Hurteau et al 2015Hurteau et al , 2017. The experiments comply with the ARRIVE guidelines (Kilkenny et al 2010) and principles of animal research established by The Journal of Physiology (Grundy, 2015).…”