Long-Lasting Working Memories of Obstacles Established by Foreleg Stepping in Walking Cats Require Area 5 of the Posterior Parietal Cortex

Abstract

Walking animals rely on working memory to avoid obstacles. One example is the stepping of the hindlegs of quadrupeds over an obstacle. In this case, the obstacle is not visible at the time of hindleg stepping, because of its position between the fore and hindlegs, and working memory must be used to avoid it. We have previously shown that this memory is very precise and surprisingly long-lasting and that it depends on the stepping of the forelegs over the obstacle for its initiation. In this study, we test the hypothesis that area 5 in the posterior parietal cortex of cats is necessary for the maintenance of this long-lasting working memory. We report that small bilateral lesions to area 5 do not affect the amplitude of normal stepping of the hindlegs over obstacles, but they profoundly reduce the long-lasting working memory of obstacles. We propose that inputs to area 5 associated with foreleg stepping initiate long-lasting activity that maintains the memory of obstacle height in another brain region to guide the hindlegs over obstacles.

Contribution of cells in the posterior parietal cortex to the planning of visually guided locomotion in the cat: effects of temporary visual interruption

“…The PPC may thus have a built-in storage capacity, which requires only periodic updating from visual input. These properties are similar to those of PPC neurons in area 5b that increase their discharge when the obstacle crosses between the forelimbs and hindlimbs, where no direct visual input is available once the obstacle passes under the head of the cat ; see also McVea et al 2009). …”

Segment-specific and state-dependent targeting accuracy of the stick insect

“…This is well above the range reported by Schütz and Dürr (Schütz and Dürr, 2011), and hence leaves enough time (on average 141±57ms; A.W., unpublished) for the neuromuscular system to transmit and process the information. However, we cannot exclude the possibility that the time point at which the placement of the foot is actually decided is later, similar to Schütz and Dürr (Schütz and Dürr, 2011), or even earlier, as has been reported for vertebrates that use visual and mechanosensory information to guide leg trajectories during walking [cat (McVea and Pearson, 2007;McVea et al, 2009;Wilkinson and Sherk, 2005), human (Mohagheghi et al, 2004;Patla and Vickers, 2003)]. In the case of humans wanting to place their foot at a specific target position, it has been reported that they fixate on this position on average two steps ahead, and at least 800-1000ms before the limb is placed on the target area (Patla and Vickers, 2003).…”

“…This information becomes particularly relevant when navigating through an unknown or irregular terrain. For cats (McVea and Pearson, 2007;McVea et al, 2009;Wilkinson and Sherk, 2005) and humans (Mohagheghi et al, 2004;Patla and Vickers, 2003) it is known that targeting of leg movements is primarily mediated by visual information that is captured on average two steps ahead. Likewise Niven and colleagues showed that locusts visually target their front legs towards the position of a ladder rung and information about the position of the rung is acquired before leg swing is initiated (Niven et al, 2010).…”

“…Cats, for example, use information from muscle receptors and cutaneous receptors in the skin to match sensory information from different joints and reliably represent the position of the limb relative to the body in the dorsal root ganglia (Stein et al, 2004). This information is also transferred to area 5 in the posterior parietal cortex where it is integrated with memorized visual information in order to perform appropriate leg movements (McVea et al, 2009), which are in turn generated in the local networks of the spinal cord (for review, see Grillner and Jessell, 2009;Kiehn et al, 2010). Similarly, it is known from work on stick insects that proprioceptive inputs of several sensory structures in the leg influence the protraction end point of all legs (Wendler, 1964;Bässler, 1977;Dean and Wendler, 1983;Cruse et al, 1984).…”

Supraspinal Control Predicts Locomotor Function and Forecasts Responsiveness to Training after Spinal Cord Injury

“…31 Corticospinal inputs further serve to modify the pattern of spinal locomotor output in situations where there is a need for control of foot placement, such as when there are constraints on the walking pattern 32 or a need to adapt gait to environmental obstacles. 33,34 Activation of red nucleus neurons and the rubrospinal tract coincides with maximal hindimb flexor electromyographical (EMG) activity and is associated with the extent of hip flexion during swing phase. [35][36][37] The lateral vestibular nucleus neurons exhibit high resting discharge rate, which establishes tonic muscle tone of paraspinal muscles extending to the lumbar cord, providing static posture and balance control.…”