Dynamic Ontogeny of Auditory Lateralization in the Zebra Finch

Functional lateralization is a ubiquitous trait in the animal kingdom and represents a general and conserved mechanism of the central nervous system. Lateralized processes observed in adult sensory cortices emerge as a function of development and experience, e.g. speech-processing in humans and processing of conspecific vocalizations in songbirds. Adult Zebra finches (ZFs), a species of songbird, exhibit right-lateralized activity in the higher auditory region caudomedial nidopallium (NCM) which depends on normal rearing conditions; auditory deprivation leads to atypical bilateral responses to conspecific song. Here, we investigate the ontogenetic timeline of auditory lateralization and the lasting effects of auditory rearing-environment in the developing ZF (40-120 days post-hatch, phd). ZFs were raised in one of three acoustic environments: 1) a tutor-playback driven paradigm, 2) chronic exposure to a ZF aviary recording (no tutor), and 3) chronic exposure to a canary aviary recording (no tutor). By longitudinally tracking lateralized auditory evoked potentials at the level of the dura, we show that adult right-lateralized activity 1) emerges from an initial left-biased profile; 2) this left-to-right emergence occurs [~]60-80phd and does not require the presence of a tutor; and 3) also emerges in ZFs raised in a canary auditory environment. Furthermore, lateralization and song development were positively correlated, although these measurements are not necessarily causally related. Awake, bilateral NCM electrophysiology in the same birds when adult, confirmed they were right-lateralized and that lateralized activity for specific test stimuli depended on rearing experience. Lastly, a decoding assay showed that canary-based rearing led to increased decoding accuracy of canary test stimuli, suggesting that neurons exhibit enhanced encodability for those sounds heard earlier. Together, the results document the ontogenetic timeline of auditory lateralization in the songbird and show that auditory experience in development, including passive exposure, shapes how auditory regions in the brain process stimuli in adulthood. Taken together with earlier results showing 1) the absence of lateral differences in ZFs reared in auditory deprivation and 2) that lateralization reverses dynamically in concert with improved discrimination in adult ZFs exposed to novel auditory environments, our current timeline suggests that the dynamic emergence of lateralization reflects the brains plastic response to novel auditory experiences. Significance StatementLateralized brain processes are ubiquitous in the animal kingdom and are shaped by sensory experience during development. Further, developmental experience can have lasting effects on adult sensory processing. Here, we document, for the first time, the timeline of the emergence of auditory lateralization in the Zebra finch and characterize the lasting effects of rearing experience on adult auditory processing in a higher auditory association region.