Periodic Reporting for period 5 - MIDNIGHT (Neural mechanism underlying vocal interactions in duetting nightingales)
Reporting period: 2023-09-01 to 2025-02-28
This project investigated the neurobiological substrates of vocal turn-taking, a complex communicative behavior requiring precise sensorimotor integration and flexible vocal responses. Utilizing the counter-singing behavior of nightingales as a model system, we aimed to elucidate the neural mechanisms underlying rapid auditory-motor mapping and context-dependent vocal adjustments.
Behavioral analyses of wild nightingales engaged in vocal interactions with playbacks revealed the capacity for instantaneous and accurate pitch imitation across their vocal repertoire suggesting a highly efficient auditory-vocal transformation pathway. Furthermore, investigation of territorial vocal exchanges demonstrated dynamic modulation of song timing and spectral features contingent upon rival identity, underscoring complex auditory processing during social communication. To probe the neural correlates of these behaviors, electrophysiological recordings were conducted in the premotor nucleus of songbirds involved in song learning and production. Complementary studies in zebra finches focused on the role of inhibitory circuits within the premotor nucleus. Selective manipulation of inhibitory interneurons in adult zebra finches, beyond the critical period for song learning, resulted in the reopening of a latent window of motor plasticity, enabling the acquisition of novel vocal syllables upon exposure to new auditory. This demonstrates a critical role for inhibitory mechanisms in regulating vocal learning and potentially in shaping the adaptive vocal responses observed during vocal turn-taking. Additionally, we found that inhibition within the premotor nucleus regulates the timing of vocal output during vocal turn taking
Collectively, these findings provide insights into the neural circuits and mechanisms underlying vocal turn-taking, highlighting the importance of rapid auditory-motor integration, context-dependent processing, and the regulatory role of inhibitory microcircuits in shaping vocal behavior.
Behavioral analyses of wild nightingales engaged in vocal interactions with playbacks revealed the capacity for instantaneous and accurate pitch imitation across their vocal repertoire suggesting a highly efficient auditory-vocal transformation pathway. Furthermore, investigation of territorial vocal exchanges demonstrated dynamic modulation of song timing and spectral features contingent upon rival identity, underscoring complex auditory processing during social communication. To probe the neural correlates of these behaviors, electrophysiological recordings were conducted in the premotor nucleus of songbirds involved in song learning and production. Complementary studies in zebra finches focused on the role of inhibitory circuits within the premotor nucleus. Selective manipulation of inhibitory interneurons in adult zebra finches, beyond the critical period for song learning, resulted in the reopening of a latent window of motor plasticity, enabling the acquisition of novel vocal syllables upon exposure to new auditory. This demonstrates a critical role for inhibitory mechanisms in regulating vocal learning and potentially in shaping the adaptive vocal responses observed during vocal turn-taking. Additionally, we found that inhibition within the premotor nucleus regulates the timing of vocal output during vocal turn taking
Collectively, these findings provide insights into the neural circuits and mechanisms underlying vocal turn-taking, highlighting the importance of rapid auditory-motor integration, context-dependent processing, and the regulatory role of inhibitory microcircuits in shaping vocal behavior.
From project start, we investigated neural mechanisms of avian vocal communication. Key achievements include: 1) Identifying the role of inhibition within a premotor circuit in precise vocal turn-taking and developing a predictive computational model. 2) Discovering that female vocal feedback drives accurate song learning in juvenile males via plasticity in the premotor nucleus. 3) Demonstrating nightingales' rapid, context-independent pitch imitation, suggesting a fundamental sensorimotor transformation. 4) Critically, showing that optogenetic disinhibition in the premotor nucleus of adult zebra finch reopens the critical period for song learning, enabling novel syllable acquisition without disrupting existing song. These results reveal fundamental principles of vocal control and learning, with implications for understanding human communication disorders and motor skill acquisition.
Our work has demonstrated the unique ability of nightingales to rapidly match pitch and adjust their songs based on context, establishing them as a novel model for studying vocal turn-taking. We also pioneered the use of Neuropixel probes for recordings in songbirds, which allowed us to reveal distinct neural representations of vocalizations. Furthermore, we achieved a scientific breakthrough by successfully reopening vocal plasticity in adult zebra finches through the manipulation of inhibitory neurons. This finding suggests a key role for inhibition in both vocal learning and turn-taking. We have also elucidated the function of specific inhibitory interneuron populations within the premotor nucleus in regulating vocal timing and enabling vocal plasticity during social interactions. To integrate these findings, we developed a computational model that provides a comprehensive understanding of the neuronal basis of vocal turn-taking. Our ongoing work will focus on characterizing the neural circuits underlying rapid auditory-motor mapping and context-dependent vocal responses in nightingales using Neuropixel recordings and intracellular techniques.