From hand to mouth: monkeys require greater effort in motor preparation for voluntary control of vocalization than for manual actions

Abstract

Voluntary control of vocal production is an essential component of the language faculty, which is thought to distinguish humans from other primates. Recent experiments have begun to reveal the capability of non-human primates to perform vocal control; however, the mechanisms underlying this ability remain unclear. Here, we revealed that Japanese macaque monkeys can learn to vocalize voluntarily through a different mechanism than that used for manual actions. The monkeys rapidly learned to touch a computer monitor when a visual stimulus was presented and showed a capacity for flexible adaptation, such that they reacted when the visual stimulus was shown at an unexpected time. By contrast, successful vocal training required additional time, and the monkeys exhibited difficulty with vocal execution when the visual stimulus appeared earlier than expected; this occurred regardless of extensive training. Thus, motor preparation before execution of an action may be a key factor in distinguishing vocalization from manual actions in monkeys; they do not exhibit a similar ability to perform motor preparation in the vocal domains. By performing direct comparisons, this study provides novel evidence regarding differences in motor control abilities between vocal and manual actions. Our findings support the suggestion that the functional expansion from hand to mouth might be a critical evolutionary event for the acquisition of voluntary control of vocalizations.