The Multiple Representations of Complex Digit Movements in Primary Motor Cortex Form the Building Blocks for Complex Grip Types in Capuchin Monkeys.

In the present study, we investigated motor cortex (M1) and a small portion of premotor and parietal cortex using intracortical microstimulation in anesthetized capuchin monkeys. Capuchins are the only New World monkeys that have evolved an opposable thumb and use tools in the wild. Like most Old World monkeys and humans, capuchin monkeys have highly dexterous hands. We surveyed a large extent of M1 and found that ~22% of all evoked movements in M1 involved the digits, and the majority of these consisted of finger flexions and extensions. Different subtypes of movements could be identified, including opposable movements of digits 1 and 2 (D1 and D2). Interestingly, the pattern of such movements varied between animals. In one case, movements involved the adduction of the medial surface of D1 toward the lateral surface of D2, whereas in the other case, the tips of D1 and D2 came in contact. Unlike other primates examined, we also found extensive representations of the prehensile foot and tail. We propose that the manual behavioral repertoire of capuchin monkeys, which includes the use of tools in the wild, is well represented within the motor cortex in the form of muscle synergies between different body parts that compose these larger, complex behaviors.SIGNIFICANCE STATEMENT The ability to use tools is a milestone in human evolution. Capuchin monkeys are one of the few non-human primates that use tools in the wild. The present study is the first detailed exploration of the motor cortex of these primates using long-train intracortical microstimulation. Within primary motor cortex, we evoked finger movements involving flexions and extensions of multiple digits, or of the first and second digits alone. Interestingly, flexion of tail and toes could also be evoked. Together, these results suggest that the functional organization of the motor cortex represents not just muscles of the body, but muscle synergies that form the building blocks of the complex behavioral repertoire of these animals.

Thalamic Inputs to Posterior Parietal Cortical Areas Involved in Skilled Forelimb Movement and Tool Use in the Capuchin Monkey.

The posterior parietal cortex (PPC) is a central hub for the primate forebrain networks that control skilled manual behavior, including tool use. Here, we quantified and compared the sources of thalamic input to electrophysiologically-identified hand/forearm-related regions of several PPC areas, namely areas 5v, AIP, PFG, and PF, of the capuchin monkey (Sapajus sp). We found that these areas receive most of their thalamic connections from the Anterior Pulvinar (PuA), Lateral Posterior (LP) and Medial Pulvinar (PuM) nuclei. Each PPC area receives a specific combination of projections from these nuclei, and fewer additional projections from other nuclei. Moreover, retrograde labeling of the cells innervating different PPC areas revealed substantial intermingling of these cells within the thalamus. Differences in thalamic input may contribute to the different functional properties displayed by the PPC areas. Furthermore, the observed innervation of functionally-related PPC domains from partly intermingled thalamic cell populations accords with the notion that higher-order thalamic inputs may dynamically regulate functional connectivity between cortical areas.