Modeling of cellular environments with nanofabricated biomaterial scaffolds has the potential to improve growth and functional development of cultured cellular models, as well as assist in tissue engineering efforts. An understanding of how such substrates may alter cellular function is critical. Highly plastic central nervous system hippocampal cells and non-network forming peripheral nervous system dorsal root ganglion cells from embryonic rats were cultured upon laminin coated degradable polycaprolactone and non-degradable polystyrene electrospun nanofibrous scaffolds with fiber diameters similar to those of neuronal processes. The two cell types displayed intrinsically different growth patterns on the nanofibrous scaffolds. Hippocampal neurites grew both parallel and perpendicular to the nanofibers, a property that would increase neurite-to-neurite contacts and maximise potential synapse development, essential for extensive network formation in a highly plastic cell type. In contrast, non-network-forming dorsal root ganglion neurons grew neurites exclusively along fibers, recapitulating the simple direct unbranching pathway between sensory ending and synapse in the spinal cord that occurs in vivo. In addition, the two primary neuronal types showed different functional capacities under patch clamp testing. Substrate composition did not alter neuronal functional development, supporting electrospun polycaprolactone and polystyrene as candidate materials for controlled cellular environments in culture and electrospun polycaprolactone for directed neurite outgrowth in tissue engineering applications.