The spiral ganglion is a compelling model system to examine how morphological form contributes to sensory function. While the ganglion is composed mainly of a single class of type I neurons that make simple one‐to‐one connections with inner hair cell sensory receptors, it has an elaborate overall morphological design. Specific features, such as soma size and axon outgrowth, are graded along the spiral contour of the cochlea. To begin to understand the interplay between different regulators of neuronal morphology, we cocultured neuron explants with peripheral target tissues removed from distinct cochlear locations. Interestingly, these “hair cell microisolates” were capable of both increasing and decreasing neuronal somata size, without adversely affecting survival. Moreover, axon characteristics elaborated de novo by the primary afferents in culture were systematically regulated by the sensory endorgan. Apparent peripheral nervous system (PNS)‐like and central nervous system (CNS)‐like axonal profiles were established in our cocultures allowing an analysis of putative PNS/CNS axon length ratios. As predicted from the in vivo organization, PNS‐like axon bundles elaborated by apical cocultures were longer than their basal counterparts and this phenotype was methodically altered when neuron explants were cocultured with microisolates from disparate cochlear regions. Thus, location‐dependent signals within the organ of Corti may set the “address” of neurons within the spiral ganglion, allowing them to elaborate the appropriate tonotopically associated morphological features in order to carry out their signaling function. J. Comp. Neurol. 524:2182–2207, 2016. © 2015 Wiley Periodicals, Inc. Co‐cultures of spiral ganglion neurons (SGN, red) and organ of Corti (dotted line) reveal that tonotopic elements of the in vivo structure can regenerate in vitro. Additionally, a “transition zone” (arrowheads) forms that could serve to separate the distinctive PNS (line) and CNS cell phenotypes and molecular markers (synaptophysin, green).