Neuromechanical strategies for obstacle negotiation during overground locomotion following an incomplete spinal cord injury in adult cats

Abstract

Following incomplete spinal cord injury in animals, including humans, substantial locomotor recovery can occur. However, functional aspects of locomotion, such as negotiating an obstacle remains challenging. We collected kinematic and electromyography data in ten adult cats before and at weeks 1-2 and 7-8 after a lateral mid-thoracic hemisection while they negotiated obstacles of three different heights. Intact cats always cleared obstacles without contact. At weeks 1-2 after hemisection, the ipsilesional hindlimb contacted obstacles in ~50% of trials, triggering a stumbling corrective reaction or lack of response. When complete clearance occurred, we observed exaggerated ipsilesional hindlimb flexion when it crossed the obstacle with the contralesional limbs leading. At weeks 7-8 after hemisection, complete clearance increased in favor of absent responses while the proportion of stumbling corrective reactions remained relatively the same. We found redistribution of weight support after hemisection, with reduced diagonal supports and increased homolateral supports, particularly on the contralesional side. The main neural strategy for complete clearance in intact cats consisted of increased activation of muscles that flex the knee. After hemisection, knee flexor activation remained but it was insufficient or more variable as the limb approached the obstacle. Intact cats also increased their speed when stepping over an obstacle, an increase that disappeared after hemisection. The increase in complete clearance over time after hemisection paralleled the recovery of muscle activation patterns or new strategies. Our results suggest partial recovery of anticipatory control through neuroplastic changes in the locomotor control system.

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).…”

“…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.…”

Spinal sensorimotor circuits play a prominent role in hindlimb locomotor recovery after staggered thoracic lateral hemisections but cannot restore posture and interlimb coordination during quadrupedal locomotion in adult cats

“…Cats were not trained to recover quadrupedal locomotion but data collection included several treadmill tasks, such as tied-belt locomotion from 0.4 to 1.0 m/s and split-belt locomotion (left slow/right fast and right slow/left fast), with both the right and left sides stepping on the slow and fast belts (Lecomte et al, 2022). Cats also performed overground locomotion in a straight line and in turns on a custom-built walkway, as well as obstacle negotiations (Lecomte et al, 2023). Some projects also included having cats walk on different surfaces (e.g., foam) to evaluate the influence of somatosensory feedback.…”

“…Our study followed ARRIVE guidelines for animals studies (Percie du Sert et al, 2020). As part of our effort to reduce the number of animals used in research, all cats participated in other studies to answer different scientific questions, some of which have been published (Lecomte et al, 2022(Lecomte et al, , 2023Merlet et al, 2022).…”

“…At the end of the experiments, cats were anesthetized with isoflurane before receiving a lethal dose (100 mg/kg) of pentobarbital through the left or right cephalic vein. The extent of the spinal lesion was confirmed by histology, as described previously (Lecomte et al, 2022(Lecomte et al, , 2023. Following euthanasia, a 2 cm length of the spinal cord centered on the lesion sites was dissected and placed in 25 mL of 4% paraformaldehyde solution (PFA in 0.1 m PBS, 4°C).…”