A lifetime of neurogenesis in the olfactory system

Jessica H Brann, Stuart J Firestein, Jessica H Brann, Stuart J Firestein

Abstract

Neurogenesis continues well beyond embryonic and early postnatal ages in three areas of the nervous system. The subgranular zone supplies new neurons to the dentate gyrus of the hippocampus. The subventricular zone supplies new interneurons to the olfactory bulb, and the olfactory neuroepithelia generate new excitatory sensory neurons that send their axons to the olfactory bulb. The latter two areas are of particular interest as they contribute new neurons to both ends of a first-level circuit governing olfactory perception. The vomeronasal organ and the main olfactory epithelium comprise the primary peripheral olfactory epithelia. These anatomically distinct areas share common features, as each exhibits extensive neurogenesis well beyond the juvenile phase of development. Here we will discuss the effect of age on the structural and functional significance of neurogenesis in the vomeronasal and olfactory epithelia, from juvenile to advanced adult ages, in several common model systems. We will next discuss how age affects the regenerative capacity of these neural stem cells in response to injury. Finally, we will consider the integration of newborn neurons into an existing circuit as it is modified by the age of the animal.

Keywords: aging; proliferation; regeneration; renewal; stem cell.

Figures

Figure 1
Figure 1
Organization and zones of the mouse olfactory epithelium. (A) Sagittal schematic of the rodent nose depicting the locations of the olfactory epithelium and the vomeronasal organ (VNO). (B) The VNO is a bilaterally symmetrical tubular structure; shown here is one half of a coronal plane as it would appear through the depth of this structure. The marginal zones (M) are found at the extreme dorsal (D) and ventral (V) regions of the VNO. Adjacent to the marginal zones are the intermediate zones (I). In between the two intermediate zones is the central zone (Ce). OB, Olfactory bulb; OE, olfactory epithelium; B, blood vessel; C, caudal; L, lumen; R, rostral. Reprinted with permission from the Journal of Neuroscience (Brann and Firestein, 2010). (C) The olfactory epithelia are composed of five primary cell types, including the horizontal basal cell (HBC), globose basal cell (GBC), immature olfactory sensory neuron (OSNi), mature olfactory sensory neuron (OSNm), and sustentacular cell (Sus).
Figure 2
Figure 2
The effect of organismal age on the rate of neurogenesis. (A) The number of cells incorporating BrdU per mm in the rodent declines precipitously over the first month of life, but reaches a steady-state level in the adult that does not appear to be profoundly affected by aging. Graph of the authors' calculations from Wilson and Raisman (1980); Weiler et al. (1999); Weiler (2005); Brann and Firestein (2010), normalized to peak value reported. (B) The neurogenic response of the OE following lesion (bulbectomy). Figure is adapted from Kastner et al. (2000). Cell number (blue dashed line, filled circles), number of apoptotic cells (black dashed line, filled squares), and cells incorporating 3H-thymidine (red solid line, triangles) in the olfactory epithelium of mice expressed relative to their respective maxima. The levels of mitotic cells (red) peak 5 days post-surgery, while total cell number (dotted line) is at its lowest following surgery.

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