Parenchymal precursor cells act in concert with canonical neural progenitors to facilitate neural circuit recovery following neuronal loss

Seasonal environmental variation represents one of the most pervasive and recurring forces shaping the vertebrate brain through cycles of neural circuit plasticity and remodeling that ultimately serves to maintain adaptive behavior. Although the contribution of adult neurogenesis to such remodeling is well-characterized across vertebrates, the role of astrocytes in supporting or enabling this process remains almost entirely unknown. Here, using the robust and natural seasonal loss of neurons within the sensorimotor nucleus HVC of the songbird, we identify a rapid astrocytic turnover event following neuronal loss and reveal a previously undescribed cellular mechanism supporting neural circuit recovery. Using lineage-specific and proliferation labeling, we establish the presence of a previously undescribed SOX2-positive neural progenitor-like population residing within the vertebrate parenchyma, outside the canonical ventricular zone niche. These parenchymal astrocyte precursor cells (pAPCs) maintain quantifiable, steady-state proliferation under homeostatic conditions, yet expand in pool size following seasonally-driven neuronal loss. The coordinated response of canonical neural progenitor cells and pAPCs produces new astrocytes that persist throughout the re-establishment of homeostasis. These findings reveal extensive astrocyte plasticity in the adult vertebrate brain, operating across both canonical and non-canonical progenitor niches, and challenge the prevailing view that parenchymal astrocytes are largely post-mitotic outside of injury contexts. More broadly, our findings establish a framework for understanding how glial populations contribute to neural circuit resilience both to the physiological and neural changes that recurring seasonal transitions drive, and to the accelerating environmental changes that increasingly challenge the adaptive capacity of animal brains worldwide.