Dynamics of lateralized electrophysiological and cellular processes in the zebra finch auditory system
Creators: name: Cataldo, Basilio Furest
Publisher: name: No Publisher Supplied
Year: 2025

description: Songbirds provide a powerful model for studying adult neuroplasticity in the auditory cortex as a function of recent auditory experience due to many parallels with the human auditory system, which is similarly tasked with processing complex conspecific vocalizations. As in human speech processing, lateralized auditory responses are evident in the songbird’s higher auditory cortex, NCM (caudomedial nidopallium), which encodes stimulus-specific auditory memories through a process of adaptation that leads to reduced responses to familiar sounds. The right NCM typically shows larger auditory responses and adaptation rates than the left for conspecific song, suggesting lateral differences in auditory representations and memory; this pattern of lateralization is known to depend on normal rearing conditions, however the ontogeny or the stability of auditory lateralization in adulthood have not been explored. Furthermore, the songbird brain incorporates new neurons in adulthood, including in NCM. In a series of coordinated experiments, Zebra Finches (ZFs; Taeniopygia guttata) were used to explore the effects of auditory exposure on learning and lateralized NCM responses via electrophysiology, immunohistochemistry, and behavioral assays. 1) we show that adult-like, right-lateralized auditory responses emerge out of left-biased patterns about halfway through development and that auditory experience in development shapes NCM responses in adulthood. 2) we document the time course of changes in lateralized auditory responses in adult ZFs exposed to a foreign, heterospecific (canary) acoustic environment; these changes are characterized as shifts in lateralization, whereby lateralization transiently reverses to a left-biased state, followed by a return to the original right-biased state after prolonged exposure; finches that experienced both the reversal and return to typical right-lateralized patterns of activity exhibited enhanced ability to behaviorally discriminate between test stimuli (canary songs). 3) these dynamic changes in the pattern of lateralized activity are shown to occur successively when ZFs are sequentially exposed to two different heterospecific environments (canary and budgerigar); in addition, we characterize how exposure to these environments leads to learning at the neural level (multiunit and single-unit in NCM). 4) we show that the shifts in lateralized activity manifest at the cellular level and potentially at different loci of the auditory afferent pathway. Furthermore, the exposure paradigm elicits shifts in the lateral distribution of new neurons in NCM, suggesting a possible neural substrate of lateralized neuroplasticity. 5) Finally, we provide evidence for learning in ZFs exposed to a heterospecific environment for different durations, using a novel behavioral method that explores learning in a consequence-free head-turning assay, Together, the results suggest that lateralization represents the current state of an organism, whereby adult-like lateralization is maintained by the current stimulus statistics, and dramatic changes in the stimulus statistics reverts the brain to a learning (developmental-like) state out of which (re)emerges the adult-like state; further, these changes in lateralization states are observed in loci along the afferent auditory pathway and we propose that they are a read-out of neurobiological substrates of learning.