Harnessing vocal patterns for social communication

Abstract

Work on vocal communication, influenced by a drive to understand the evolution of language, has focused on auditory processing and forebrain control of learned vocalizations. The actual hindbrain neural mechanisms used to create communication signals are understudied, in part because of the difficulty of experimental studies in species that rely on respiration for vocalization. In these experimental systems-including those that embody vocal learning-vocal behaviors have rhythmic qualities. Recent studies using molecular markers and 'fictive' patterns produced by isolated brains are beginning to reveal how hindbrain circuits generate vocal patterns. Insights from central pattern generators for respiration and locomotion are illuminating common neural and developmental mechanisms. Choice of vocal patterns is responsive to socially salient input. Studies of the vertebrate social brain network suggest mechanisms used to integrate socially salient information and produce an appropriate vocal response.

Fig. 1

A. Hindbrain rhombomeres are specified from anterior to posterior by a Hox code; here each Hox gene is indicated by a different pastel-colored bar (note that the code can be combinatorial). Hox genes are a sub-set of homeotic genes implicated in segmental identities. The branchial arches and forelimbs are innervated by neurons whose axons form the caudal cranial nerves. Based on [17]. B. Transverse sections through the hindbrain at levels from R4 to R8. Groups of interneurons are organized in stripes (indicated by brightly colored bars; these do not match part A) and can be identified by expression of transcription factors and genes associated with neurotransmitter identity (modified from[16]). Abbreviation: R, rhombomere.

Fig. 2

A. and B. An underwater microphone records advertisement calling in a male X. laevis and an en passant electrode records vocal nerve activity (compound action potentials) [32]. C. Components of the neural pathway for call production in X. laevis. The hindbrain VPG includes nucleus DTAM rostrally and interneurons at the anterior pole of nucleus (n.) IX–X caudally. DTAM and vocal motor neurons express androgen receptor (AR). In the forebrain, the amygdala (AMY) expresses receptor for gonadotropin (GTR) and projects to DTAM. Modified from [54]. D. Recordings of a local field potential (highlighted in yellow) from DTAM in the isolated brain (in blue) reveal activity that mirrors the fictive advertisement call pattern recorded from the vocal nerve (lower panel; figure by C. Barkan). Abbreviations: AMY, amygdala; DTAM, used as a proper noun; n. IX–X, nucleus ambiguus, VMN, vocal motor nerve.

Fig. 3

Swimming in X. laevis tapoles and the swim CPG. Both interneurons and motor neurons participate in this motor pattern. Rohon-beard sensory neurons, stimulated by touch, activate excitatory dla and dlc neurons, which in turn, stimulate dINs to control the rhythmic output of the motor neurons (MNs). Commisural cIN interneurons coordinate unilateral flexion through contralateral inhibition. Inhibitory aINs regulate high frequency swimming and inhibit sensory activation (modified from [47, 53]).