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, 36 (48), 12168-12179

Distinct Neural Activities in Premotor Cortex During Natural Vocal Behaviors in a New World Primate, the Common Marmoset (Callithrix Jacchus)

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Distinct Neural Activities in Premotor Cortex During Natural Vocal Behaviors in a New World Primate, the Common Marmoset (Callithrix Jacchus)

Sabyasachi Roy et al. J Neurosci.

Abstract

Although evidence from human studies has long indicated the crucial role of the frontal cortex in speech production, it has remained uncertain whether the frontal cortex in nonhuman primates plays a similar role in vocal communication. Previous studies of prefrontal and premotor cortices of macaque monkeys have found neural signals associated with cue- and reward-conditioned vocal production, but not with self-initiated or spontaneous vocalizations (Coudé et al., 2011; Hage and Nieder, 2013), which casts doubt on the role of the frontal cortex of the Old World monkeys in vocal communication. A recent study of marmoset frontal cortex observed modulated neural activities associated with self-initiated vocal production (Miller et al., 2015), but it did not delineate whether these neural activities were specifically attributed to vocal production or if they may result from other nonvocal motor activity such as orofacial motor movement. In the present study, we attempted to resolve these issues and examined single neuron activities in premotor cortex during natural vocal exchanges in the common marmoset (Callithrix jacchus), a highly vocal New World primate. Neural activation and suppression were observed both before and during self-initiated vocal production. Furthermore, by comparing neural activities between self-initiated vocal production and nonvocal orofacial motor movement, we identified a subpopulation of neurons in marmoset premotor cortex that was activated or suppressed by vocal production, but not by orofacial movement. These findings provide clear evidence of the premotor cortex's involvement in self-initiated vocal production in natural vocal behaviors of a New World primate.

Significance statement: Human frontal cortex plays a crucial role in speech production. However, it has remained unclear whether the frontal cortex of nonhuman primates is involved in the production of self-initiated vocalizations during natural vocal communication. Using a wireless multichannel neural recording technique, we observed in the premotor cortex neural activation and suppression both before and during self-initiated vocalizations when marmosets, a highly vocal New World primate species, engaged in vocal exchanges with conspecifics. A novel finding of the present study is the discovery of a subpopulation of premotor cortex neurons that was activated by vocal production, but not by orofacial movement. These observations provide clear evidence of the premotor cortex's involvement in vocal production in a New World primate species.

Keywords: marmoset; premotor; vocalization; wireless.

Figures

Figure 1.
Figure 1.
Illustrations of the experimental setup and examples of recorded marmoset vocalizations. A, Schematic illustration of the recording chamber with acoustic and wireless neural recording systems. HS, Wireless head stage; Rx, receiver. The custom-built chamber was designed to isolate electromagnetic wave transmission and reflection, attenuate external sounds, and reduce internal sound reflection (Roy and Wang, 2012). In the vocal production condition, an experimental subject was placed in a plastic cage shown on the left side of the chamber. A wireless headstage (HS) was mounted on top of the subject's head and connected to an electrode array in the premotor cortex. A receiver (Rx) for the wireless system was placed above the cage. The subject's vocalizations were recorded by a microphone in front of the cage. During antiphonal calling behavior, a virtual conspecific was configured on the right side of the chamber. It replaced a real marmoset by a computer-controlled playback system and engaged the experimental subject in vocal exchanges (Miller et al., 2009). B, Computer algorithm controlling the virtual conspecific (Miller and Wang 2006; Miller et al., 2009). Once a phee call from the experimental subject was detected, a prerecorded phee of another marmoset in our colony was presented by the playback system with a delay (1–5 s, according to the statistics of antiphonal calling delays between pairs of marmosets). If there was no response from the experimental subject, another prerecorded phee was presented after a second delay (up to 60 s, according to the statistics of the time intervals between spontaneously produced phee calls). C, Spectrogram showing a series of antiphonal phee exchanges. In this example, the experimental subject made single-phrase phee calls and the virtual conspecific delivered two-phrase phee calls. D, Estimated electrode coverage areas for the three hemispheres (with Brodmann's areas marked accordingly). The area between 6DC and 6Va is 8C. The colored square is aligned with the outermost electrodes of the array. Locations of electrode arrays are estimated based on histology (6207A) and geometric measurements on the skull surface during implantation (with respect to the lateral sulcus) with a comparison with the marmoset brain atlas (Paxinos et al., 2012). Scale bar, 5 mm. The turquoise arrow indicates the approximate location of the example section in E. LH, left hemisphere; RH, Right hemisphere. E, Coronal sections from 6207A right hemisphere with cytochrome oxidase stain. Top, Example section marked with cortical regions (border indicated with arrowheads) and electrode locations (asterisks). The approximate location of the section with respect to the brain on the rostral–caudal axis is indicated by a turquoise arrow in D. Bottom, Series of sections from the frontal brain of 6207A with the border of the electrode coverage area marked (dashed line). D–V, Dorsal–ventral; C–R, caudal–rostral.
Figure 2.
Figure 2.
Neural activity in the vocal production condition: examples of individual neurons for individual recording sessions. A, Neuron showing increased activity before vocal onset. Top, Each vertical line indicates a spike. Spike timing is aligned to the vocal onset. Orange bars indicate the duration of phee call phrases. Some of the calls had two phrases, which are shown as two bars in a row. In general, subjects tended to make multiphrase phee calls at the beginning of an experimental session and were more likely to produce single-phrase phee calls toward the end. Bottom, Firing rate shown as mean ± SEM. N indicates the number of calls. B, Neuron showing decreased activity during vocal production. This neuron was recorded in the same vocal production session as the neuron in A. C, Neuron showing increased activity near the vocal onset time. Three analysis windows are used to capture neuronal activities as in these examples: pre-, post-, and peri- windows, indicated by a red bar and a pink-shaded area (AC). The spont-window used in analysis is indicated by a green bar and shaded area (AC). D, Neuron showing decreased activity before vocal onset and increased activity during vocal production. E, Same neuron in D, with only single-phrase phee calls included. A clear activation is also seen after the end of the vocal production. F, Neuron showing strong activation both before and during vocal production.
Figure 3.
Figure 3.
Neural activity in the vocal production condition: population average across neurons with different types of modulations in the pre-window and post-window. A, Population-averaged normalized firing rates of neurons showing activation in the pre-window regardless of modulation type in other windows (mean ± SEM). Firing rates are normalized as z-score for each neuron by the baseline firing rate in the spont-window and then averaged across the neurons. The number of neurons in the population is indicated by n. The shaded bars indicate the average durations of each phee call phrase. C, E, Same format as A for groups of neurons with no modulation (C) and suppression (E) in the pre-window. B, D, F, Same format as A for groups of neurons with activation (B), no modulation (D), and suppression (F) in the post-window.
Figure 4.
Figure 4.
Summary of neuron distributions in different experimental conditions and response categories. A, Total of 332 single neurons were tested in the vocal production condition from marmosets 35U right hemisphere and 6207A right hemisphere (Table 1). A subset of these neurons (282/332) were also tested in the playback condition. A further subset of those neurons (267/282) were tested in the orofacial movement condition (licking), as illustrated by the Venn diagram. A total of 255 of the 267 neurons tested in all three conditions showed no responses to the playback vocalizations and were classified into four categories (vocal-only, vocal-orofacial, orofacial-only, and no modulation). B, Estimated electrode locations (marked by red dots) of the arrays implanted on two hemispheres (top, 35U right hemisphere; bottom, 6207A right hemisphere) are overlaid on a published marmoset brain atlas (Paxinos et al., 2012). Recordings were made from 15 of 16 electrodes in each array (one electrode in each array was used as the reference and is not marked). The number next to each red dot indicates the number of vocal-only neurons found at that electrode location (no number shown if none was found). Recording locations in premotor region are marked by green-shaded area and those in the border region are marked by yellow-shaded area. Of 255 neurons recorded from both hemispheres, 213 were from the premotor region and 42 were from the border region. The number of neurons in each of the four categories (vocal-only, vocal-orofacial, orofacial-only, and no modulation) are 20 (9.4%), 116 (54.5%), 57 (26.8%), and 20 (9.4%) for the premotor region and 3 (7.1%), 22 (52.4%), 16 (38.1%), and 1 (2.4%) for the border region, respectively.
Figure 5.
Figure 5.
Population-averaged normalized firing rates (z-score, mean ± SEM) of the vocal-only neurons in each of the three experimental conditions. A, B, Vocal production. C, D, Orofacial movement (licking). E, F, Playback. The vocal-only neurons are separated into two groups, activated (A, C, E) and suppressed (B, D, F) in the vocal production condition. The shaded bars indicate the average durations of each phee call phrase (A, B, E, F) or averaged duration of the licking (C, D).
Figure 6.
Figure 6.
Neural activities related to orofacial movement (licking). A, Example neuron showing increased activity during orofacial movement (licking). The orange bar in the raster plot indicates the duration of licking. B, Population-averaged normalized firing rates (z-score, mean ± SEM) of the vocal-orofacial neurons in two experimental conditions, vocal production (top) and orofacial movement (licking; bottom). The shaded bars indicate the average durations of each phee call phrase (top) or averaged duration of the licking (bottom). C, Population-averaged normalized firing rates (z-score, mean ± SEM) of the orofacial-only neurons in orofacial movement (licking) condition. The shaded bar indicates the average duration of the licking.
Figure 7.
Figure 7.
Comparisons of the normalized firing rates (z-score) between vocal production and orofacial movement conditions. The comparisons are made for the four categories of neurons, respectively, as defined in Figure 4 in two analysis windows: pre-window (A) and post-window (B). y-axis is the vocal production condition; x-axis is the orofacial movement (licking) condition. A few data points with z-scores outside of the [−5,10] range are plotted on the border of the axes.

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