Cellular Organization and Migration Pathways of the Ventricular–Subventricular Zone in the Juvenile Swine Brain (Sus scrofa domesticus)

Abstract

The ventricular–subventricular zone (V-SVZ), lining the lateral walls of the lateral ventricles, is a major neurogenic region in the adult brain of many mammals. This study investigates the structural organization and cellular composition of the V-SVZ in the juvenile swine brain (3–5 months), providing novel insights into neuroblast migration in gyrencephalic species. Using immunohistochemistry combined with transmission and scanning electron microscopy, we redefined the cytoarchitecture of the swine V-SVZ, identifying four distinct cellular layers. Layer 1 consists of a pseudostratified epithelium of glial fibrillary acidic protein-positive ependymal cells, whose cilia and microvilli extend into the ventricular lumen, frequently surrounding supraependymal axons. Beneath it, layer 2 is composed of astrocytic and radial glia processes and contains occasional clusters of doublecortin (DCX)-positive cells with prominent microtubules and elongated cytoplasm, indicative of a migratory phenotype. Layer 3 is further subdivided into a low-cell-density sublayer 3a, enriched with myelinated axons and scattered DCX⁺ clusters, and a high-cell-density sublayer 3b, characterized by large groups of DCX⁺ migratory cells. In sagittal sections, these cells form long chains oriented parallel to the ventricular surface. Neuroblasts emerging from the dorsal V-SVZ migrate caudorostrally through the rostral migratory stream toward the olfactory bulb. The layered organization of the swine V-SVZ resembles that of humans, where DCX⁺ chains persist up to 18 months of age, positioning the swine as a valuable model for investigating postnatal plasticity and neurogenic potential in gyrencephalic brains. The persistence of immature neurons in the V-SVZ of gyrencephalic mammals, including infant humans, underscores the relevance of this region for neurogenesis and plasticity in large-brained species.