We tested the hypothesis that area 5 of the posterior parietal cortex (PPC) contributes to the planning of visually guided gait modifications. We recorded 121 neurons from the PPC of two cats during a task in which cats needed to process visual input to step over obstacles attached to a moving treadmill belt. During unobstructed locomotion, 64/121 (53%) of cells showed rhythmic activity. During steps over the obstacles, 102/121 (84%) of cells showed a significant change of their activity. Of these, 46/102 were unmodulated during the control task. We divided the 102 task-related cells into two groups on the basis of their discharge when the limb contralateral to the recording site was the first to pass over the obstacle. One group (41/102) was characterized by a brief, phasic discharge as the lead forelimb passed over the obstacle (Step-related cells). These cells were recorded primarily from area 5a. The other group (61/102) showed a progressive increase in activity prior to the onset of the swing phase in the modified limb and frequently diverged from control at least one step cycle before the gait modification (Step-advanced cells). Most of these cells were recorded in area 5b. In both groups, some cells maintained a fixed relationship to the activity of the contralateral forelimb regardless of which limb was the first to pass over the obstacle (limb-specific cells), whereas others changed their phase of activity so that they were always related to activity of the first limb to pass over the obstacle, either contralateral or ipsilateral (limb-independent cells). Limb-independent cells were more common among the Step-advanced cell population. We suggest that both populations of cells contribute to the gait modification and that the discharge characteristics of the Step-advanced cells are compatible with a contribution to the planning of the gait modification.
We developed a novel locomotor task in which cats step over obstacles that move at a different speed from that of the treadmill on which the cat is walking: we refer to this as a visual dissociation locomotion task. Slowing the speed of the obstacle with respect to that of the treadmill sometimes led to a major change in strategy so that cats made two steps with the hindlimbs before stepping over the obstacle (double step strategy) instead of the single step (standard strategy) observed when the obstacle was at the same speed as the treadmill. In addition, in the step preceding the step over the obstacle, the paws were placed significantly closer to the obstacle in the visual dissociation task than when the treadmill and the obstacle were at the same speed. After unilateral lesion of area 5 of the posterior parietal cortex (PPC), the cats frequently hit the obstacle as they stepped over it, especially in the visual dissociation task. This locomotor deficit was linked to significant differences in the location in which the forelimbs were placed in the step preceding that over the obstacle compared with the prelesion control. Cats also frequently hit the obstacle with their hindlimbs even when the forelimbs negotiated the obstacle successfully; this suggests an important role for the posterior parietal cortex in the coordination of the forelimbs and hindlimbs. Together, these results suggest an important contribution of the PPC to the planning of visually guided gait modifications.
We tested the hypothesis that area 5 of the posterior parietal cortex (PPC) contributes to interlimb coordination in locomotor tasks requiring visual guidance by recording neuronal activity in this area in three cats in two locomotor paradigms. In the first paradigm, cats were required to step over obstacles attached to a moving treadmill belt. We recorded 47 neurons that discharged in relationship to the hindlimbs. Of these, 31/47 discharged between the passage of the fore- and hindlimbs (FL-HL cells) over the obstacle. The activity of most of these neurons (25/31) was related to the fore- and hindlimb contralateral to the recording site when the contralateral forelimb was the first to pass over the obstacle. In many cells, discharge activity was limb-independent in that it was better related to the ipsilateral limbs when they were the first to step over the obstacle. The other 16/47 neurons discharged only when the hindlimbs stepped over the obstacle with the majority of these (12/16) discharging between the passage of the two hindlimbs over the obstacle. We tested 15/47 cells, including 11/47 FL-HL cells, in a second paradigm in which cats stepped over an obstacle on a walkway. Discharge activity in all of these cells was significantly modulated when the cat stepped over the obstacle and remained modified for periods of ≤ 1 min when forward progress of the cat was delayed with either the fore- and hindlimbs, or the two hindlimbs, straddling the obstacle. We suggest that neurons in area 5 of the PPC contribute to interlimb coordination during locomotion by estimating the spatial and temporal attributes of the obstacle with respect to the body. We further suggest that the discharge observed both during the steps over the obstacle and in the delayed locomotor paradigm is a neuronal correlate of working memory.
Stepping over obstacles requires vision to guide the leading leg, but direct visual information is not available to guide the trailing leg. The neural mechanisms for establishing a stored obstacle representation and thus facilitating the trail leg trajectory in humans are unknown. Twenty-four subjects participated in one of three experiments, which were designed to investigate the contribution of visual, proprioceptive, and efference copy signals. Subjects stepped over an obstacle with their lead leg, stopped, and straddled the obstacle for a delay period before stepping over it with their trail leg while toe elevation was recorded. Subsequently, we calculated maximum toe elevation and toe clearance. First, we found that subjects could accurately scale trail leg toe elevation and clearance, despite straddling an obstacle for up to 2 min, similar to quadrupeds. Second, we found that when the lead leg was passively moved over an obstacle (eliminating an efference copy signal and altering proprioception) without vision, trail leg toe elevation and clearance were reduced, and variability increased compared with when subjects actively moved their lead leg. Trail leg toe measures returned to normal when vision was provided during the passive manipulation. Finally, we found that altering lead leg proprioceptive feedback by adding mass to the ankle had no effect on trail leg toe measures. Taken together, our results suggest that humans can store a neural representation of obstacle properties for extended periods of time and that vision appears to be sufficient in this process to guide trail leg trajectory.
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