Inhibition within a premotor circuit controls the timing of vocal turn-taking in zebra finches

Abstract

Vocal turn-taking is a fundamental organizing principle of human conversation but the neural circuit mechanisms that structure coordinated vocal interactions are unknown. The ability to exchange vocalizations in an alternating fashion is also exhibited by other species, including zebra finches. With a combination of behavioral testing, electrophysiological recordings, and pharmacological manipulations we demonstrate that activity within a cortical premotor nucleus orchestrates the timing of calls in socially interacting zebra finches. Within this circuit, local inhibition precedes premotor neuron activation associated with calling. Blocking inhibition results in faster vocal responses as well as an impaired ability to flexibly avoid overlapping with a partner. These results support a working model in which premotor inhibition regulates context-dependent timing of vocalizations and enables the precise interleaving of vocal signals during turn-taking.

Vocal learning and flexible rhythm pattern perception are linked: Evidence from songbirds

“…In songbirds, a premotor nucleus that controls song timing (25) has reciprocal connections with forebrain auditory regions (19,62). Predictive activity in this region has been reported prior to anticipated calls with a vocal partner (21), and damage to or inactivation of the motor pathway interferes with temporally precise vocal turn taking (22,23). These results are consistent with the notion that interactions between vocal motor and auditory regions may generate predictive timing signals that facilitate flexible rhythm perception.…”

“…More recently, predictive activity in the song motor pathway prior to anticipated calls has been reported during social call exchanges (21). Finally, several studies have shown that zebra finches can predict the timing of isochronous, antiphonal calls during vocal turn taking and can adjust their own call timing to avoid interference, an ability that is disrupted by manipulations of the song motor pathway (21)(22)(23). Taken together, these results are consistent with the notion that interactions between vocal motor and auditory regions may generate predictive timing signals that facilitate flexible rhythm perception.…”

Neurotelemetry Reveals Putative Predictive Activity in HVC during Call-Based Vocal Communications in Zebra Finches

“…The stack call-related premotor activity of HVC interneurons is corroborated by recent results ( Benichov and Vallentin, 2020 ). For singing, structured activity of interneurons is thought to provide permissive time windows for the activity of the descending premotor neurons, which leads to a sequential motor pattern ( Kosche et al, 2015 ).…”

Songbirds can learn flexible contextual control over syllable sequencing

“…individually targeted syllable transitions) in response to arbitrarily assigned contextual stimuli that have no prior ethological relevance. (Vignal, Mathevon, & Mottin, 2004), to enhance communication, or to avoid overlap or 'jamming' during vocal turn-taking and in response to environmental noises (Benichov & Vallentin, 2020;Brumm & Zollinger, 2013). Such ethologically relevant capacities for vocal control likely reflect evolutionary advantages of incorporating sensory and contextual information about conspecifics and the environment in generating increasingly sophisticated vocal signaling.…”

“…Even birds with only a single song type, such as Bengalese finches, vary parameters of their song depending on social context, including the specific identity of the listener (Chen et al, 2016;Heinig et al, 2014;Sakata et al, 2008). The ability to contextually control vocalizations is also relevant for the customization of vocal signatures for purposes of individual and group recognition (Vignal, Mathevon, & Mottin, 2004), and to avoid overlap and enhance communication during vocal turn-taking and in response to environmental noises (Benichov & Vallentin, 2020;Brumm & Zollinger, 2013). Such capacities for vocal control likely reflect evolutionary advantages of incorporating sensory and contextual information about conspecifics and the environment in generating increasingly sophisticated vocal signaling.…”