Neurons controlling voluntary vocalization in the macaque ventral premotor cortex

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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. © 2011 Coudé et al.

Figures

  • Figure 1. Vocal operant conditioning task. A. Top. Each trial consisted in a ‘‘Food’’ (green) and a ‘‘No Food’’ (red) condition. Bottom. Schematic illustration of a successful trial of the task. In the ‘‘Food’’ condition the food was presented on a table (1); if the monkey emitted a coo (2), the food was given to the monkey that grasped it (3) and brought it to the mouth (4). In the ‘‘No Food’’ condition the food was not present and the monkey was not required to vocalize (5). B. Monkeys performance throughout baseline and training phases. Each dot of the line graph represents the average percentage of the performance on three consecutive training sessions. For the sake of clarity only the sessions taken from the onset, middle and end of each training phase are shown. Black dots = successful vocalization trials; empty dots = vocalization trials in which SV occurred. C. Percentage of trials with vocalization in ‘‘Food’’ and ‘‘No Food’’ conditions for the two monkeys. Error bars represent s.e.m. doi:10.1371/journal.pone.0026822.g001
  • Figure 2. Recorded region and vocalization-selective neurons. A. Left. Lateral view of the left hemisphere of Monkey 2. Colored sectors indicate hand (blue), mouth (red) and overlapping hand and mouth (purple) motor representations. Right. Enlarged view of the recorded area showing the position of electrode penetrations (white dots) where vocalization-selective neurons were found. Note that some penetrations overlapped. cs = central sulcus, ias = inferior arcuate sulcus, ps = principal sulcus. B. Examples of three vocalization-selective neurons recorded during four different behaviors. For each unit, rasters and histograms illustrate the neuronal discharge aligned (vertical gray line) with behavioral events. They correspond to monkey sound emission onset during vocalization, contact with food during biting and maximum lips protrusion during silent vocalization (SV). During rest, the activity alignment corresponded to the midpoint of a period in which the monkey did not produce any movement. The root mean square of sound trace of monkey vocalization is depicted for each unit above the response raster related to vocalization. C. Frequency of vocalization-selective (black bars) and vocalization/mouth related neurons (white bars) according to discharge time onset with respect to the beginning of sound emission. doi:10.1371/journal.pone.0026822.g002
  • Table 1. Number of neurons responding during trained vocalization.
  • Figure 4. Representation of the penetrations in PMv in which long-train microstimulation evoked larynx, mouth and tongue movements. Other conventions as in Fig. 2. doi:10.1371/journal.pone.0026822.g004

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APA

Coudé, G., Ferrari, P. F., Rodà, F., Maranesi, M., Borelli, E., Veroni, V., … Fogassi, L. (2011). Neurons controlling voluntary vocalization in the macaque ventral premotor cortex. PLoS ONE, 6(11). https://doi.org/10.1371/journal.pone.0026822

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