Identifying the Neural Dynamics that Orchestrate Vocal Interactions in Zebra Finches

• Applicant: Jonathan Benichov, Ph.D.
• Subject Area: Cognitive, Systems and Behavioural Neurobiology
• Term: from 2020 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 459524793

An enjoyable conversation effortlessly flows back and forth between speakers. While we typically focus on the ideas being shared, we often take for granted the extraordinary act of coordination that structures these exchanges. Specifically, vocally interacting with a partner involves perceiving relevant acoustic signals and initiating specific motor commands to generate an appropriate vocal reply. This auditory-vocal interplay occurs during spoken conversations, but it is also the basis of the phylogenetically widespread phenomenon of vocal turn-taking. In the simplest form, each interlocutor delays or withholds utterances while listening to the other and responds once they stop. This social sensorimotor coordination reduces acoustic overlap, thereby maintaining unmasked signal transmission and detection. The neural mechanisms that coordinate the timing of vocal responses to social sounds are largely unexplored. I plan to investigate this fundamental form of vocal control in the zebra finch. In this gregarious songbird species, all individuals exchange and can temporally coordinate short innate calls. As part of my Ph.D. work, I developed a behavioral assay for eliciting, disrupting, and quantifying vocal coordination in zebra finch call interactions. I have expanded on this approach during my post-doc by pairing this vocally interactive behavioral paradigm with intracellular electrophysiological recordings and pharmacological perturbations within a premotor circuit to highlight the influence of local inhibition on call timing. In studying the neural basis of vocal coordination in zebra finches, it has been essential for me to use minimally-encumbering electrophysiological recording methods to measure neuronal activity along with the vocal output of interacting individuals. In the proposed work, I plan to apply my knowledge of awake-behaving electrophysiological recordings in zebra finches to trace the auditory influences on interactive vocal timing. Specifically, I will record multiunit neuronal activity across a primary sensorimotor vocal center and the upstream nucleus that serves as its greatest source of higher-order auditory inputs. Measuring and inducing changes in activity across these two regions while birds listen to and produce social vocalizations will clarify how vocal coordination emerges from a sensorimotor pathway. The specific aims of my proposed research project are as follows: 1) To characterize the effects of temporal predictability and social familiarity of heard calls on call response behavior. 2) To determine how hearing partners’ social acoustic signals affects activity in a premotor vocal circuit. And 3) to trace the sequence of neural activity from auditory processing to precisely-timed vocal production during interactions.

• DFG Programme: Research Grants