Neurogenesis in the vomeronasal epithelium of adult garter snakes. 2. Reconstitution of the bipolar neuron layer following experimental vomeronasal axotomy

Abstract

Postnatal neurogenesis and reconstitution of the neuronal layer of the vomeronasal epithelium have been demonstrated in adult garter snakes following vomeronasal axotomy. Two weeks following axotomy the vomeronasal epithelium was depleted of its bipolar layer but the basal, undifferentiated cells were actively proliferating. In subsequent weeks the undifferentiated cell layer continued to increase its cell population through mitosis and began to occupy the neuron-depleted zone of the receptor cell column. Four weeks following axotomy the denervated epithelium contained an expanded Ud cell layer which occupied the basal one-half to two-thirds of the receptor cell column. The cells at the base of the expanded Ud cell layer were morphologically similar to Ud cells in a normal epithelium whereas the cells at the apex of the columns resembled normal differentiating neurons. A few necrotic cells could still be detected within the apical, cell-depleted zone. By the eighth post-operative week the receptor cell column was fully occupied with cells formed as a result of Ud cell proliferation. The most apical cells, 6-10 cells deep, were morphologically similar to normal bipolar neurons with a dendritic process reaching the lumen of the VN organ. The remaining cells were morphologically similar to normal differentiating or Ud cells. Sixteen weeks following axotomy a larger portion of cells in the receptor cell column were fully differentiated bipolar neurons. The Ud cell population was reduced and, as in the normal epithelium, occupied only the basal portion of each receptor cell column. The regenerated neurons of the VNO were capable of synthesizing and transporting macromolecules to the telencephalon as demonstrated by autoradiography following intraepithelial injections of [3H]proline. Newly formed axons terminated in the accessory olfactory bulb within 8 weeks following axotomy. These results support the view that the basal Ud cells were the source of neurons in the regenerating vomeronasal organ and demonstrate a dynamic process of neuronal proliferation, differentiation and maturation in the denervated vomeronasal epithelia of adult garter snakes.