Hybrid dedicated and distributed coding in PMd/M1 provides separation and interaction of bilateral arm signals

Pronounced activity is observed in both hemispheres of the motor cortex during preparation and execution of unimanual movements. The organizational principles of bi-hemispheric signals and the functions they serve throughout motor planning remain unclear. Using an instructed-delay reaching task in monkeys, we identified two components in population responses spanning PMd and M1. A “dedicated” component, which segregated activity at the level of individual units, emerged in PMd during preparation. It was most prominent following movement when M1 became strongly engaged, and principally involved the contralateral hemisphere. In contrast to recent reports, these dedicated signals solely accounted for divergence of arm-specific neural subspaces. The other “distributed” component mixed signals for each arm within units, and the subspace containing it did not discriminate between arms at any stage. The statistics of the population response suggest two functional aspects of the cortical network: one that spans both hemispheres for supporting preparatory and ongoing processes, and another that is predominantly housed in the contralateral hemisphere and specifies unilateral output.Author summary: The motor cortex of the brain primarily controls the opposite side of the body, yet neural activity in this area is often observed during movements of either arm. To understand the functional significance of these signals we must first characterize how they are organized across the neural network. Are there patterns of activity that are unique to a single arm? Are there other patterns that reflect shared functions? Importantly, these features may change across time as motor plans are developed and executed. In this study, we analyzed the responses of individual neurons in the motor cortex and modeled their patterns of co-activity across the population to characterize the changes that distinguish left and right arm use. Across preparation and execution phases of the task, we found that signals became gradually more segregated. Despite many neurons modulating in association with either arm, those that were more dedicated to a single (typically contralateral) limb accounted for a disproportionately large amount of the variance. However, there were also weaker patterns of activity that did not distinguish between the two arms at any stage. These results reveal a heterogeneity in the motor cortex that highlights both independent and interactive components of reaching signals.