TheXenopusAmygdala Mediates Socially Appropriate Vocal Communication Signals

Abstract

Social interaction requires that relevant sensory information is collected, classified, and distributed to the motor areas that initiate an appropriate behavioral response. Vocal exchanges, in particular, depend on linking auditory processing to an appropriate motor expression. Because of its role in integrating sensory information for the purpose of action selection, the amygdala has been implicated in social behavior in many mammalian species. Here, we show that two nuclei of the extended amygdala play essential roles in vocal communication in the African clawed frog, Xenopus laevis. Transport of fluorescent dextran amines identifies the X. laevis central amygdala (CeA) as a target for ascending auditory information from the central thalamic nucleus and as a major afferent to the vocal pattern generator of the hindbrain. In the isolated (ex vivo) brain, electrical stimulation of the CeA, or the neighboring bed nucleus of the stria terminalis (BNST), initiates bouts of fictive calling. In vivo, lesioning the CeA of males disrupts the production of appropriate vocal responses to females and to broadcasts of female calls. Lesioning the BNST in males produces an overall decrease in calling behavior. Together, these results suggest that the anuran CeA evaluates the valence of acoustic cues and initiates socially appropriate vocal responses to communication signals, whereas the BNST plays a role in the initiation of vocalizations.

Evolution of vocal patterns: tuning hindbrain circuits during species divergence

“…DTAM also receives input from the central amygdala located in the ventral forebrain (Brahic and Kelley, 2003;Hall et al, 2013). Because previous work has also shown that removal of the midbrain and forebrain does not disrupt fictive calling in X. laevis (Yu and Yamaguchi, 2010), we predicted that species-specific LFP wave patterns are generated autonomously within the hindbrain compartment that includes DTAM.…”

Comparative Neurobiology of Sound Production in Fishes

“…As reviewed below, the essential developmental evidence across vertebrate lineages to support comparisons of a hindbrain CPG for patterning the activity of sonic muscles (larynx, syrinx, swim bladder) first became available only during the past few years . This led to the renaming of the sonic motor nucleus that innervates swim bladder muscles as the vocal motor nucleus, or VMN , a nomenclature that is followed here and has recently been adopted by studies of the amphibian laryngeal system (Hall et al 2013). …”

Harnessing vocal patterns for social communication

“…Fictive calling – a pattern of nerve compound action potentials (CAPs) that matches temporal features recorded during actual calling [32; Fig. 2B] – can be reliably evoked in an isolated brain by raising endogenous serotonin using reuptake inhibitors, by serotonin application or by stimulating the amygdala [33–35]. Vocal pattern generating circuitry is contained within the hindbrain and includes a more rostral, rhythmically active group of neurons located in the dorsal medulla at the level of cranial nerve V (DTAM, used as a proper noun) as well as interneurons and laryngeal motor neurons in the caudal hindbrain.…”

“…Taken together, these results indicate that hormone-sensitive vocal initiation must arise upstream of the hindbrain VPG. A strong candidate for initiation is a forebrain nucleus, the amygdala, that receives auditory input and innervates elements of the VPG [35] as described below.…”

“…The amygdala receives input from auditory thalamus. When the amygdala is lesioned, males do not produce socially-appropriate vocal responses to call broadcasts [35]. They respond to female rapping and ticking as though to the call of another male (i.e.…”