Neuromechanical Strategies for Obstacle Negotiation during Overground Locomotion following 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 obstacles remains challenging. We collected kinematic and electromyography data in ten adult cats (5 males, 5 females) before and at weeks 1-2 and 7-8 after a lateral mid-thoracic hemisection on the right side of the cord while they negotiated obstacles of three different heights. Intact cats always cleared obstacles without contact. At weeks 1-2 after hemisection, the ipsilesional right hindlimb contacted obstacles in ∼50% of trials, triggering a stumbling corrective reaction or absent responses, which we termed Other. When complete clearance occurred, we observed exaggerated ipsilesional hindlimb flexion when crossing the obstacle with contralesional left limbs leading. At weeks 7-8 after hemisection, the proportion of complete clearance increased, Other responses decreased, and stumbling corrective reactions remained relatively unchanged. We found redistribution of weight support after hemisection, with reduced diagonal supports and increased homolateral supports, particularly on the left contralesional side. The main neural strategy for complete clearance in intact cats consisted of increased knee flexor activation. After hemisection, ipsilesional 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.Significance statement:Most spinal cord injuries (SCI) are incomplete and people can recover some walking functions. However, the main challenge for people with SCI that do recover a high level of function is to produce a gait that can adjust to everyday occurrences, such as turning, stepping over an obstacle, etc. Here, we use the cat model to answer two basic questions: How does an animal negotiate an obstacle after an incomplete SCI and why does it fail to safely clear it? We show that the inability to clear an obstacle is because of improper activation of muscles that flex the knee. Animals recover a certain amount of function thanks to new strategies and changes within the nervous system.

Spinal interneuron population dynamics underlying flexible pattern generation

“…While we identified that the hold region was an important state space feature in governing the duration of extensor burst during air stepping, we acknowledge that the utility of this feature may not be apparent or implemented across all behaviors. Behaviors that are dominated by flexor-muscle activity or require more variation in the duration of the swing phase (e.g., obstacle avoidance, (Lecomte et al, 2023)) may require different mechanisms to generate that type of motor output variability that we did not observe in the spinal cat during air-stepping. Additionally, the extension bias we observed may also be attributed in part due to the experimental conditions (i.e., spinalized animal, clonidine-induced, air stepping with no ground reaction forces).…”

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).…”

“…Cardiac arrest was confirmed using a stethoscope to determine the death of the animal. Spinal cords were then harvested for histological analysis (Audet et al, 2023;Lecomte et al, 2023).…”

“…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.…”

Forelimb movements contribute to hindlimb cutaneous reflexes during locomotion in cats

“…Proper integration of cutaneous feedback within central neural circuits is required to execute specific motor tasks and perform necessary movement corrections. For instance, during locomotion, when the foot dorsum contacts an obstacle during the swing phase, a coordinated reflex response, termed the stumbling corrective reaction, allows the perturbed limb to step away from and over the obstacle to avoid falling, as shown in cats and humans (Forssberg et al 1977; Forssberg 1979; Frigon et al 2021; Haridas and Zehr 2003; Lecomte et al 2023; Merlet et al 2022; Prochazka et al 1978; Quevedo et al 2005a; Schillings et al 1996; Van Wezel et al 1997; Zehr et al 1997). Electrically stimulating cutaneous nerves of the foot also elicits a coordinated reflex response, consistent with the stumbling corrective reaction in cats and humans (Buford and Smith 1993; Forssberg 1979; Haridas and Zehr 2003; Lam et al 2003; Potocanac et al 2016; Prochazka et al 1978; Quevedo et al 2005a, 2005b; Schillings et al 2000, 2005; Van Wezel et al 1997; Wand et al 1980; Zehr et al 1997).…”