Widespread neuronal activity related to bimanual coordination in non-human primates: evidence from Fos-like activation during bimanual versus unimanual motor task.

Abstract

Electrophysiological data support the notion that spatial and temporal coordination between the forelimbs in primates takes place in a wide network of cortical and subcortical brain structures. However, single neuron electrophysiology is biased towards large, long distance projecting neurons. The aim of the present study was to assess whether the same neural network is involved when small and medium size neurons are considered. To address this issue, neuronal activity with cellular resolution was investigated and quantified using the c-fos mapping technique, targeting small and medium size diameter neurons, in adult non-human primates. Two male macaque monkeysⁱ were trained to perform a reach and grasp drawer task, executed either bimanually (BIM) or unimanually (UNI). Extensive single unit electrophysiological recordings were conducted in these two monkeys over a two-year period, preceding a final terminal c-fos session during which one monkey (Mk-1) performed exclusively the BIM task, while the second monkey (Mk-2) performed the UNI task only (250 trials each). One additional monkey (control Mk-3) did not perform any task. Fos-like immunoreactivity (FLI) was significantly higher in both Mk-1 and Mk-2 in motor brain areas than in the control monkey, demonstrating that motor activity triggered c-fos. Although the overall muscle activity was roughly comparable in both tasks, Mk-1 (BIM) exhibited a clearly stronger FLI than Mk-2 all along the rostrocaudal axis of the primary, supplementary and cingulate motor cortices, as well as the striatum. In contrast, Mk-1 and Mk-2 displayed a comparable FLI in non-motor regions, such as the visual and auditory thalamus. The present study, a very rare c-fos mapping investigation conducted in macaques performing a complex behavioral task, suggests that small and medium size (local) neurons may also contribute to the specific neural activity responsible for precise interlimb coordination, within a network associating motor cortical areas and the basal ganglia.