Abstract
The voluntary control of phonation is a crucial achievement in the evolution of speech. In humans, ventral premotor cortex (PMv) and Broca's area are known to be involved in voluntary phonation. In contrast, no neurophysiological data are available about the role of the oro-facial sector of nonhuman primates PMv in this function. In order to address this issue, we recorded PMv neurons from two monkeys trained to emit coo-calls. Results showed that a population of motor neurons specifically fire during vocalization. About two thirds of them discharged before sound onset, while the remaining were time-locked with it. The response of vocalization-selective neurons was present only during conditioned (voluntary) but not spontaneous (emotional) sound emission. These data suggest that the control of vocal production exerted by PMv neurons constitutes a newly emerging property in the monkey lineage, shedding light on the evolution of phonation-based communication from a nonhuman primate species.
Highlights
Nonhuman primates vocalize in a wide range of contexts and possess a repertoire of vocalizations used to designate objects, events or affective states [1,2]
Due to this apparent lack of flexibility, nonhuman primate vocal behavior was traditionally assumed to be predominantly emotional [7,8,9], and consisting in a repertoire of involuntary or reflexive responses to a range of specific valence stimuli [10,11]. Conflicting with this view, behavioral studies showed that macaques can have a limited control on vocalization. Demonstrated that they can achieve a significant level of voluntary vocal control when submitted to operant conditioning tasks [6,12,13,14], even though the success rate obtained in those studies is highly variable [15,16]
The number of silent vocalization’’ (SV) rose, together with the number of actual vocalizations, suggesting that this behavior is a failed attempt to vocalize. This idea is in line with the fact that this gesture does not correspond to any other known pig-tail macaque communicative facial expression and that it was never observed in untrained monkeys housed in our facility
Summary
Nonhuman primates vocalize in a wide range of contexts and possess a repertoire of vocalizations used to designate objects, events or affective states [1,2]. Some species are capable of modifying their vocalizations according to environmental parameters [3,4,5], none of them is granted with enough flexibility to learn completely new vocal patterns (see [6]). Due to this apparent lack of flexibility, nonhuman primate vocal behavior was traditionally assumed to be predominantly emotional [7,8,9], and consisting in a repertoire of involuntary or reflexive responses to a range of specific valence stimuli [10,11]. Demonstrated that they can achieve a significant level of voluntary vocal control when submitted to operant conditioning tasks [6,12,13,14], even though the success rate obtained in those studies is highly variable [15,16]
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