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Vocalization Induced CFos Expression in Marmoset Cortex

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Vocalization Induced CFos Expression in Marmoset Cortex

Cory T Miller et al. Front Integr Neurosci.

Abstract

All non-human primates communicate with conspecifics using vocalizations, a system involving both the production and perception of species-specific vocal signals. Much of the work on the neural basis of primate vocal communication in cortex has focused on the sensory processing of vocalizations, while relatively little data are available for vocal production. Earlier physiological studies in squirrel monkeys had shed doubts on the involvement of primate cortex in vocal behaviors. The aim of the present study was to identify areas of common marmoset (Callithrix jacchus) cortex that are potentially involved in vocal communication. In this study, we quantified cFos expression in three areas of marmoset cortex - frontal, temporal (auditory), and medial temporal - under various vocal conditions. Specifically, we examined cFos expression in these cortical areas during the sensory, motor (vocal production), and sensory-motor components of vocal communication. Our results showed an increase in cFos expression in ventrolateral prefrontal cortex as well as the medial and lateral belt areas of auditory cortex in the vocal perception condition. In contrast, subjects in the vocal production condition resulted in increased cFos expression only in dorsal premotor cortex. During the sensory-motor condition (antiphonal calling), subjects exhibited cFos expression in each of the above areas, as well as increased expression in perirhinal cortex. Overall, these results suggest that various cortical areas outside primary auditory cortex are involved in primate vocal communication. These findings pave the way for further physiological studies of the neural basis of primate vocal communication.

Keywords: auditory cortex; common marmoset; frontal cortex; immediate early gene expression; medial temporal cortex; vocal communication.

Figures

Figure 1
Figure 1
(A) Schematic drawing of the marmoset cortex. For our analysis we divided the frontal cortex, defined as the area of cortex rostral to motor cortex, into three regions (1, 2, 3) along the rostral–caudal plane and two areas along the dorsal/ventrolateral plane. These divisions are shown in the drawing. For both B and C, the three behavioral conditions are plotted (Antiphonal – black diamond; Vocal Perception – open gray circle; Vocal Production – filled gray circle). (B) Figure plot the mean percentage of immunoreactive neurons in the dorsal (above) area of the frontal cortex. Data are shown for each of the three frontal regions (1–3). (C) Figure plot the mean percentage of immunoreactive neurons in the ventrolateral area of the frontal cortex. Data are shown for each of the three frontal regions (1–3).
Figure 2
Figure 2
Shows an example of an immunoreactive neuron viewed at the same magnification (100×) and window size (50 μm × 50 μm) that all stereology analyses were performed.
Figure 3
Figure 3
The number of immunoreactive neurons in the frontal cortex. (A–C) Data from the three behavioral conditions are shown in box plots for the dorsal and ventrolateral areas for Frontal Regions 1–3. Each box plot shows the median and upper and lower quartiles; the whiskers plot the range. Statistically significant p-values for One-way ANOVA tests comparing cFos expression across the behavioral conditions within a region are noted. “*” denotes significant differences in paired comparisons. (Ant, Antiphonal calling; Perc, Vocal perception; Prod, Vocal production).
Figure 4
Figure 4
(Top) A schematic drawing of the auditory cortex. The locations of the Medial Belt, Core, and Lateral Belt are highlighted. (A–C) Bar graphs plot the mean # of immunoreactive neurons measured in the three behavioral conditions in each of these three areas of the auditory cortex. Statistically significant differences are noted. [Ant, Antiphonal calling (gray bar); Perc, Vocal perception (black bar); Prod, Vocal production (white bar)].
Figure 5
Figure 5
(Top) A schematic drawing of the auditory cortex. The anatomical locations of the fields within the (A) Medial Belt (RTM, RM, CM), (B) Core (RT, R, A1), and (C) Lateral Belt (RTL, AL, ML) are shown. (A–C) Data from the three behavioral conditions are shown in box plots for each of the nine auditory cortical fields measured here. Each box plot shows the median and upper and lower quartiles; the whiskers plot the range. Statistically significant p-values for One-way ANOVA tests comparing cFos expression across the behavioral conditions within a region are noted. “*” denotes significant differences in paired comparisons. (Ant, Antiphonal calling; Perc, Vocal perception; Prod, Vocal production).
Figure 6
Figure 6
The number of immunoreactive neurons in the medial temporal cortex. (Top) A schematic coronal section of the medial temporal cortex areas examined here. (Below) Data from the three behavioral conditions are shown in box plots for each of the five medial temporal cortex areas measured here. Each box plot shows the median and upper and lower quartiles; the whiskers plot the range. Statistically significant p-values for One-way ANOVA tests comparing cFos expression across the behavioral conditions within a region are noted. * – denotes significant differences in paired comparisons. (Ant, Antiphonal calling; Perc, Vocal perception; Prod, Vocal production).
Figure 7
Figure 7
Summary of results. Schematic drawings of the areas of the marmoset cortex from which IEG expression was measured here. The drawing of the whole marmoset cortex to the left shows the Frontal Cortex and Auditory Cortex, while the schematic of the medial temporal cortex is shown to the right. Circles placed in each of the individual areas reflect the mean number of immunoreactive neurons measured. The number of immunoreactive neurons each circle size represents is shown in the key at the top right. Data are shown for each of the test conditions: (A) Antiphonal Calling, (B) Vocal Perception, and (C) Vocal Production.

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