Sensory coding and sensitivity to local estrogens shift during critical period milestones in the auditory cortex of male songbirds

Abstract

Vocal learning occurs during an experience-dependent, age-limited critical period early in development. In songbirds, vocal learning begins when presinging birds acquire an auditory memory of their tutor’s song (sensory phase) followed by the onset of vocal production and refinement (sensorimotor phase). Hearing is necessary throughout the vocal learning critical period. One key brain area for songbird auditory processing is the caudomedial nidopallium (NCM), a telencephalic region analogous to mammalian auditory cortex. Despite NCM’s established role in auditory processing, it is unclear how the response properties of NCM neurons may shift across development. Moreover, communication processing in NCM is rapidly enhanced by local 17β-estradiol (E2) administration in adult songbirds; however, the function of dynamically fluctuating E2 in NCM during development is unknown. We collected bilateral extracellular recordings in NCM coupled with reverse microdialysis delivery in juvenile male zebra finches (Taeniopygia guttata) across the vocal learning critical period. We found that auditory-evoked activity and coding accuracy were substantially higher in the NCM of sensory-aged animals compared to sensorimotor-aged animals. Further, we observed both age-dependent and lateralized effects of local E2 administration on sensory processing. In sensory-aged subjects, E2 decreased auditory responsiveness across both hemispheres; however, a similar trend was observed in age-matched control subjects. In sensorimotor-aged subjects, E2 dampened auditory responsiveness in left NCM but enhanced auditory responsiveness in right NCM. Our results reveal an age-dependent physiological shift in auditory processing and lateralized E2 sensitivity that each precisely track a key neural “switch point” from purely sensory (pre-singing) to sensorimotor (singing) in developing songbirds.