Memory-Guided Stumbling Correction in the Hindlimb of Quadrupeds Relies on Parietal Area 5

Abstract

In complex environments, tripping over an unexpected obstacle evokes the stumbling corrective reaction, eliciting rapid limb hyperflexion to lift the leg over the obstruction. While stumbling correction has been characterized within a single limb in the cat, this response must extend to both forelegs and hindlegs for successful avoidance in naturalistic settings. Furthermore, the ability to remember an obstacle over which the forelegs have tripped is necessary for hindleg clearance if locomotion is delayed. Therefore, memory-guided stumbling correction was studied in walking cats after the forelegs tripped over an unexpected obstacle. Tactile input to only one foreleg was often sufficient in modulating stepping of all four legs when locomotion was continuous, or when hindleg clearance was delayed. When obstacle height was varied, animals appropriately scaled step height to obstacle height. As tactile input without foreleg clearance was insufficient in reliably modulating stepping, efference, or proprioceptive information about modulated foreleg stepping may be important for producing a robust, long-lasting memory. Finally, cooling-induced deactivation of parietal area 5 altered hindleg stepping in a manner indicating that animals no longer recalled the obstacle over which they had tripped. Altogether, these results demonstrate the integral role area 5 plays in memory-guided stumbling correction.

Stable Delay Period Representations in the Posterior Parietal Cortex Facilitate Working-Memory-Guided Obstacle Negotiation

“…However, neurons exhibiting sustained delay period modulation represent a specialized subset of area 5 neurons capable of maintaining stable representations of obstacle infor-mation in WM. As previous work demonstrated WM deficits precluding successful avoidance when a comparable region of area 5 was deactivated [9,10,28], neurons capable of stable WM maintenance are most likely necessary for such behaviors.…”

“…For example, area 5 neurons that respond to passive joint manipulation are even more responsive during active movements, demonstrating an integration of both sensory and motor inputs [40]. Correspondingly, previous work has demonstrated that, in comparison to trials where the animal is delayed just before the forelegs have stepped over an obstacle, obstacle memory is more robust when the animal is delayed after foreleg clearance [10,41]. These studies suggest that efference copies of motor commands for elevated foreleg stepping, the resulting proprioceptive feedback, or both are important for WM-guided obstacle locomotion.…”

“…To assess the neural correlates of this behavior, 32-channel floating microelectrode arrays (electrode lengths: 0.9-1.5 mm) were chronically implanted in the same region of area 5 that, when deactivated, elicits WM deficits (Figures 1C and 1D) [9,10,28]. One array was placed in area 5 of each hemisphere for both animals.…”

“…Obstacle WM was assessed by comparing obstructed (OP) with unobstructed (OA) locomotion using the same apparatus described previously [8][9][10]. In OP trials, each animal approached and stepped over a 25.8 cm wide x 8.7 cm high x 3 mm thick obstacle raised onto the surface of the walkway ( Figure 1A).…”

“…When walking resumes, elevated hindleg stepping observed even after delays tested up to 10 min demonstrates a robust, long-lasting WM of the obstacle used to guide hindleg clearance. We previously used cooling-induced cortical deactivations [7,8] to demonstrate the role of the posterior parietal cortex (PPC) in this WM-guided behavior [9,10]. When deactivations are temporally restricted to the delay during which obstacle information must be retained, WM deficits precluding successful obstacle avoidance implicates parietal area 5 in WM maintenance.…”