Tucker, W. C.; Shepard, S. L.; Chambers, P. E.; Majji, A.; Boyd, J. M.; Larson, T. A.

Songbirds exhibit remarkable seasonal neuroplasticity, with song control nuclei undergoing seasonal cycles of extreme and rapid neuronal death and regeneration. While adult neurogenesis in these systems is well-characterized, the dynamics and functional significance of astrocytic turnover remain unknown. Here, we examined the fate of neural progenitor cell progeny born during seasonally-induced reactive proliferation and identified a rapid astrocytic turnover event in HVC following seasonal neuronal loss. Using lineage-specific and proliferation labeling, we characterized a previously undescribed SOX2-positive neural progenitor-like population within the avian parenchyma beyond the canonical ventricular zone niche. These parenchymal astrocyte precursor cells (pAPCs) proliferate at quantifiable, steady levels under homeostatic conditions, yet as a proliferative cell pool dramatically expand following non-injury induced neuronal death. Beyond their proliferative potential, pAPCs demonstrate capabilities suggestive of self-renewal and generation of astrocytes and neurons. The coordinated response of canonical neural progenitor cells and the newly-described pAPCs generates new astrocytes that persist throughout re-establishment of homeostasis, all of which together likely facilitate subsequent circuit regrowth. These findings reveal extensive astrocyte plasticity in the adult avian telencephalon and establish a foundation for understanding how astrocytes and their precursors - both within and beyond their canonical niches - contribute to neural circuit remodeling and behavioral maintenance.