The neurobiology of vocal communication in marmosets

Abstract

An increasingly popular animal model for studying the neural basis of social behavior, cognition, and communication is the common marmoset (Callithrix jacchus). Interest in this New World primate across neuroscience is now being driven by their proclivity for prosociality across their repertoire, high volubility, and rapid development, as well as their amenability to naturalistic testing paradigms and freely moving neural recording and imaging technologies. The complement of these characteristics set marmosets up to be a powerful model of the primate social brain in the years to come. Here, we focus on vocal communication because it is the area that has both made the most progress and illustrates the prodigious potential of this species. We review the current state of the field with a focus on the various brain areas and networks involved in vocal perception and production, comparing the findings from marmosets to other animals, including humans.

Keywords: Callithrix jacchus; neurobiology; neuroethology; social behavior; vocal communication.

FIGURE 1

Vocal behavior and neurobiology of marmosets. A) Graphical depiction of a marmoset. B) Representative spectrograms of the four most common call types are shown, recorded from a freely-moving marmoset performing natural behaviors using a wearable microphone. C) Schematic of the brain areas involved in vocal communication in marmosets. Top left is sagittal view of a marmoset brain, with the frontal cortex, auditory cortex, and temporal lobe highlighted. Top right shows a detailed view of the frontal cortex (after ^,), with areas expressed either in common name (where applicable), or Brodmann area number. Area 45 and 47 are part of the ventrolateral prefrontal cortex and area 46 is part of the dorsolateral prefrontal cortex. Bottom left shows a detailed view of a sagittal cross section of the medial temporal cortex at 3.75 mm from the midline (after ^,). . Bottom right shows a detailed view of the auditory cortex (after ), with colors indicating core (pink), belt (purple), and parabelt (blue). Abbreviations: A1, primary auditory cortex; AL, anterolateral; CL, caudolateral; CM, caudomedial; CPB, caudal parabelt; DG, dentate gyrus; M1, primary motor area; HC, hippocampus (includes Cornu Ammonis subfields CA1, CA2, and CA3); ML, middle lateral; MM, middle medial; R, rostral field; RM, rostromedial; RPB, rostral parabelt; RT, rostrotemporal; RTL, rostrotemporal lateral; RTM, rostrotemporal medial; SMA, supplementary motor area.

FIGURE 2

Cortical networks for vocal perception. A graphical representation of sensory networks involved in processing vocalizations. The MGB in the thalamus projects to the auditory cortex. From the anterior part of the auditory cortex, projections to the vlPFC are made, which represents the antero-ventral stream, while the posterior part projects onto the dlPFC, which represents the postero-dorsal stream. Abbreviations: dlPFC, dorsolateral prefrontal cortex; IC, inferior colliculus; MGB, medical geniculate body; vlPFC, ventrolateral prefrontal cortex.

FIGURE 3

Cortical networks for vocal production. A graphical representation of the three vocal production networks discussed in this review. The PVMN, or CPG and drive levels, (solid arrows) involve connections from the ACC to PAG to RF, which projects to the motoneurons. The VAMN, or environment level, (dotted arrows) shows the connection from area 45 (Broca’s area) and the vlPFC on the lateral surface to the ACC on the medial surface. The connectivity described by Cerkevich et al. (dashed arrows) involves direct connections from M1, SMA, and the ventral premotor cortex to the RF, with the two premotor connections being stronger (represented by thicker lines). Abbreviations: ACC, anterior cingulate cortex; CPG, central pattern generator; M1, primary motor cortex; PAG, periaqueductal grey; PVMN, primary vocal motor network; RF, reticular formation; SMA, supplementary motor area; VAMN, volitional articulatory motor network; vlPFC, ventrolateral prefrontal cortex.