Exploring the Consistent Roles of Motor Areas Across Voluntary Movement and Locomotion.

Multiple cortical motor areas are critically involved in the voluntary control of discrete movement (e.g., reaching) and gait. Here, we outline experimental findings in nonhuman primates with clinical reports and research in humans that explain characteristic movement control mechanisms in the primary, supplementary, and presupplementary motor areas, as well as in the dorsal premotor area. We then focus on single-neuron activity recorded while monkeys performed motor sequences consisting of multiple discrete movements, and we consider how area-specific control mechanisms may contribute to the performance of complex movements. Following this, we explore the motor areas in cats that we have considered as analogs of those in primates based on similarities in their cortical surface topology, anatomic connections, microstimulation effects, and activity patterns. Emphasizing that discrete movement and gait modification entail similar control mechanisms, we argue that single-neuron activity in each area of the cat during gait modification is compatible with the function ascribed to the activity in the corresponding area in primates, recorded during the performance of discrete movements. The findings that demonstrate the premotor areas' contribution to locomotion, currently unique to the cat model, should offer highly valuable insights into the control mechanisms of locomotion in primates, including humans.

Cortical contribution to visuomotor coordination in locomotion and reaching.

One of the hallmarks of mammals is their ability to make precise visually guided limb movements to attain objects. This is best exemplified by the reach and grasp movements of primates, although it is not unique to this mammalian order. Precise, coordinated, visually guided movements are equally as important during locomotion in many mammalian species, especially in predators. In this context, vision is used to guide paw trajectory and placement. In this review we examine the contribution of the fronto-parietal network in the control of such movements. We suggest that this network is responsible for visuomotor coordination across behaviours and species. We further argue for analogies between cytoarchitectonically similar cortical areas in primates and cats.

Uncovering and leveraging the return of voluntary motor programs after paralysis using a bi-cortical neuroprosthesis.

Rehabilitative and neuroprosthetic approaches after spinal cord injury (SCI) aim to reestablish voluntary control of movement. Promoting recovery requires a mechanistic understanding of the return of volition over action, but the relationship between re-emerging cortical commands and the return of locomotion is not well established. We introduced a neuroprosthesis delivering targeted bi-cortical stimulation in a clinically relevant contusive SCI model. In healthy and SCI cats, we controlled hindlimb locomotor output by tuning stimulation timing, duration, amplitude, and site. In intact cats, we unveiled a large repertoire of motor programs. After SCI, the evoked hindlimb lifts were highly stereotyped, yet effective in modulating gait and alleviating bilateral foot drag. Results suggest that the neural substrate underpinning motor recovery had traded-off selectivity for efficacy. Longitudinal tests revealed that the return of locomotion after SCI was correlated with recovery of the descending drive, which advocates for rehabilitation interventions directed at the cortical target.

A secondary motor area contributing to interlimb coordination during visually guided locomotion in the cat.

We investigated the contribution of cytoarchitectonic cortical area 4δc, in the caudal bank of the cruciate sulcus of the cat, to the control of visually guided locomotion. To do so, we recorded the activity of 114 neurons in 4δc while cats walked on a treadmill and stepped over an obstacle that advanced toward them. A total of 84/114 (74%) cells were task-related and 68/84 (81%) of these cells showed significant modulation of their discharge frequency when the contralateral limbs were the first to step over the obstacle. These latter cells included a substantial proportion (27/68 40%) that discharged between the passage of the contralateral forelimb and the contralateral hindlimb over the obstacle, suggesting a contribution of this area to interlimb coordination. We further compared the discharge in area 4δc with the activity patterns of cells in the rostral division of the same cytoarchitectonic area (4δr), which has been suggested to be a separate functional region. Despite some differences in the patterns of activity in the 2 subdivisions, we suggest that activity in each is compatible with a contribution to interlimb coordination and that they should be considered as a single functional area that contributes to both forelimb-forelimb and forelimb-hindlimb coordination.

Microstimulation of the Premotor Cortex of the Cat Produces Phase-Dependent Changes in Locomotor Activity.

To determine the functional organization of premotor areas in the cat pericruciate cortex we applied intracortical microstimulation (ICMS) within multiple cytoarchitectonically identified subregions of areas 4 and 6 in the awake cat, both at rest and during treadmill walking. ICMS in most premotor areas evoked clear twitch responses in the limbs and/or head at rest. During locomotion, these same areas produced phase-dependent modifications of muscle activity. ICMS in the primary motor cortex (area 4γ) produced large phase-dependent responses, mostly restricted to the contralateral forelimb or hindlimb. Stimulation in premotor areas also produced phase-dependent responses that, in some cases, were as large as those evoked from area 4γ. However, responses from premotor areas had more widespread effects on multiple limbs, including the ipsilateral limbs, than did stimulation in 4γ. During locomotion, responses in both forelimb and hindlimb muscles were evoked from cytoarchitectonic areas 4γ, 4δ, 6aα, and 6aγ. However, the prevalence of effects in a given limb varied from one area to another. The results suggest that premotor areas may contribute to the production, modification, and coordination of activity in the limbs during locomotion and may be particularly pertinent during modifications of gait.

Premotor Cortex Provides a Substrate for the Temporal Transformation of Information During the Planning of Gait Modifications.

We tested the hypothesis that the premotor cortex (PMC) in the cat contributes to the planning and execution of visually guided gait modifications. We analyzed single unit activity from 136 cells localized within layer V of cytoarchitectonic areas 6iffu and that part of 4δ within the ventral bank of the cruciate sulcus while cats walked on a treadmill and stepped over an obstacle that advanced toward them. We found a rich variety of discharge patterns, ranging from limb-independent cells that discharged several steps in front of the obstacle to step-related cells that discharged either during steps over the obstacle or in the steps leading up to that step. We propose that this population of task-related cells within this region of the PMC contributes to the temporal evolution of a planning process that transforms global information of the presence of an obstacle into the precise spatio-temporal limb adjustment required to negotiate that obstacle.