Experience- and Sex-Dependent Intrinsic Plasticity in the Zebra Finch Auditory Cortex during Song Memorization

For vocal communicators like humans and songbirds, survival and reproduction depend on highly developed auditory processing systems that can detect and differentiate nuanced differences in vocalizations, even amid noisy environments. Early auditory experience is critical to the development of these systems. In zebra finches and other songbirds, there is a sensitive period when young birds memorize a song that will serve as a model for their own vocal production. In addition to learning a specific tutor's song, the auditory system may also undergo critical developmental processes that support auditory perception of vocalizations more generally. Here, we investigate changes in intrinsic spiking dynamics among neurons in the caudal mesopallium, a cortical-level auditory area implicated in discriminating and learning species-specific vocalizations. A subset of neurons in this area only fire transiently at the onset of current injections (i.e., phasic firing), a dynamical property that can enhance the reliability and selectivity of neural responses to complex acoustic stimuli. At the beginning of the sensitive period, just after zebra finches have fledged from the nest, there is an increase in the proportion of caudal mesopallium neurons with phasic excitability, and in the proportion of neurons expressing Kv1.1, a low-threshold channel that facilitates phasic firing. This plasticity requires exposure to a complex, noisy environment and is greater in males, the only sex that sings in this species. This shift to more phasic dynamics is therefore an experience-dependent adaptation that could facilitate auditory processing in noisy, acoustically complex conditions during a key stage of vocal development.SIGNIFICANCE STATEMENT Auditory experience early in life shapes how humans and songbirds perceive the vocal communication sounds produced by their species. However, the changes that occur in the brain as this learning takes place are poorly understood. In this study, we show that in young zebra finches that are just beginning to learn the structure of their species' song, neurons in a key cortical area adapt their intrinsic firing patterns in response to the acoustic environment. In the complex, cocktail-party-like environment of a colony, more neurons adopt transient firing dynamics, which can facilitate neural coding of songs amid such challenging conditions.