Title: Auditory Tuning in Vocal Learning Songbirds
Description: Vocal learning is one of the most distinctive characteristics of the modern human species. Through the intricate interaction between vocal motor and auditory systems during early sensitive periods, humans spontaneously master the ability to speak and decode speech. Because vocal learning is so rare in vertebrates, songbirds (Oscines) are the primary model organisms used in studies of acoustic communication and vocal learning. The acquisition of songs in birds and speech in humans (learning of complex sounds with syntactic structures) exhibit similar developmental trajectories. Research on song learning has focused primarily on vocal production with limited emphasis on the role of auditory perception. While auditory tuning and sensorimotor feedback are indispensable for successful vocal learning and communication, how auditory tuning emerges at different levels of the neural processing hierarchy and how sensorimotor integration occurs in the brain during vocal learning is not fully understood.

The neurobiology research described here thus focuses on auditory tuning and sensorimotor integration in vocal learning songbirds using multiple experimental approaches. In the first chapter, I describe peripheral auditory tuning in several songbird species. Using operant conditioning, I trained individual birds to report audible tones and assessed hearing thresholds over the 0.5 to 10 kHz frequency range. I also examined the relationship between song spectral energy and hearing by analyzing song frequency-power spectra and audiograms across species. I found that across songbird species, regardless of age, rearing condition, and sex, hearing range was similar: 0.5 to 8 kHz. Notably, the vocal energy in courtship song matches each species auditory sensitivity, indicating the coevolution of sensory and vocal motor systems. In the second chapter, I describe neuronal tuning in the auditory cortex (AC) of female songbirds. While male songbirds exhibit experience-dependent neuronal tuning in AC, the nature of AC tuning in females that do not sing has not been studied.

I used in vivo acute electrophysiological recordings to examine neural responses to tones, ripple stimuli and songs. I compared neuronal firing patterns in female AC between different species groups and rearing conditions. My results suggest that higher-order auditory processing in female songbirds is conserved across species and that early song experience affects some aspects of tuning in the AC of females, suggesting that females exhibit experience-dependent changes in auditory tuning across development. In the final chapter, I examine a potential sensorimotor integration site, the caudal striatum (CSt), and its role in vocal learning. Auditory neurons in CSt suggest that the region may integrate auditory inputs and vocal motor commands to modulate sensorimotor learning. To study the effects of CSt lesions on song learning, I produced excitotoxic lesions in CSt across developmental stages. To label brain regions that project to or receive input from CSt, I injected anterograde or retrograde tracers into CSt.

I also characterized the auditory tuning properties of CSt through electrophysiological recording. I found that CSt receives both dopaminergic and auditory projections but is not necessary for successful song learning. Electrophysiological data also show that auditory tuning properties of neurons in CSt are highly similar to neurons in other AC subregions, suggesting that CSt may be a sub-region of AC.