RT Journal Article SR Electronic T1 Sensory Coding and Sensitivity to Local Estrogens Shift during Critical Period Milestones in the Auditory Cortex of Male Songbirds. JF eneuro JO eNeuro FD Society for Neuroscience SP ENEURO.0317-17.2017 DO 10.1523/ENEURO.0317-17.2017 A1 Daniel M. Vahaba A1 Matheus Macedo-Lima A1 Luke Remage-Healey YR 2017 UL http://www.eneuro.org/content/early/2017/11/30/ENEURO.0317-17.2017.abstract AB Vocal learning occurs during an experience-dependent, age-limited critical period early in development. In songbirds, vocal learning begins when pre-singing 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 region 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 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.Significance Statement Vocal communication, such as language and birdsong, is learned during an age-limited critical period early in development. Initially, infants and songbirds exclusively listen to memorize their native tongue before producing nascent vocalizations. We show that the transition from pre-singing to vocalizing in developing songbirds is accompanied by a large shift in auditory gain and coding in cortical neurons. Further, while estrogens generally improve hearing in adulthood, we found that brain estrogens either enhanced or diminished auditory responsiveness depending on both critical period phase and cerebral hemisphere. Our findings therefore highlight a neural transition in auditory processing and lateralized hormone sensitivity at a key stage in development, and similar mechanisms could be relevant for speech processing and language acquisition in humans.