Maturation and Death of Adult-Born Olfactory Bulb Granule Neurons: Role of Olfaction

By Leopoldo T. Petreanu, Arturo Alvarez-Buylla. Journal of Neuroscience, 2002

737 citations recorded by the source corpus.

Young neurons born in the subventricular zone (SVZ) of adult mice migrate to the olfactory bulb (OB) where they differentiate into granule cells (GCs) and periglomerular interneurons. Using retroviral labeling of precursors in the SVZ, we describe five stages and the timing for the maturation of newly formed GCs: (1) tangentially migrating neuroblasts (days 2–7); (2) radially migrating young neurons (days 5–7); (3) GCs with a simple unbranched dendrite that does not extend beyond the mitral cell layer (days 9–13); (4) GCs with a nonspiny branched dendrite in the external plexiform layer (days 11–22); and (5) mature GCs (days 15–30). Using [3H]thymidine, we show that the maximum number of labeled GCs is observed around day 15 after injection. Interestingly, between days 15 and 45 after birth, soon after the cells developed spines, the number of [3H]thymidine-labeled GCs declined by 50%. Using anosmic mice, we found that sensory input was critical for the survival of GCs from day 15 to 45 after labeling. However, the number and morphology of 15-d-old cells in the granule cell layer was similar in anosmic and wild-type mice. We infer that the lack of activity did not have an effect on the generation, migration, and early differentiation of granule cells. Soon after young GCs matured, and presumably became synaptically connected, their survival depended on the level of activity that they received. This selection mechanism might allow the construction of specific OB circuits based on olfactory experience and suggests possible functions of OB cell replacement.

Subfields: Developmental Neuroscience, Neurology, Sensory Systems

View Paper: https://www.semanticscholar.org/paper/c1f9062efb2629da59c0fdcdf350bb76e8ec9254

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Citations in the corpus

High Levels of Id1 Expression Define B1 Type Adult Neural Stem Cells (2009, background): “Previous studies indicate that when rapidly dividing cells are labeled by (3)H-thymidine once per day for 4 days, neuronal output peaks at 15 days then drops until 45 days (Petreanu and Alvarez-Buylla, 2002).”
The developing brain and neural plasticity: Implications for normality, psychopathology, and resilience. (2015, background): “Because olfactory cues are critical for survival, the function of the newly born olfactory neurons may be to help enhance olfactory discrimination (Petreanu & Alvarez-Buylla, 2002).”
Adult neurogenesis and cellular brain repair with neural progenitors, precursors and stem cells (2006, background): “…while the precise function of new neurons in the olfactory bulb is not yet known, one theory is that high turnover of receptor neurons in the olfactory epithelium requires a similar degree of plasticity at the level of the synaptic targets in the olfactory bulb (Petreanu & Alvarez-Buylla 2002).”
Mechanisms and functional implications of adult neurogenesis. (2008, neutral): “Newborn neurons in the olfactory bulb also go through distinct stages of development (Figures 3 and 4) (Lledo et al., 2006; Petreanu and Alvarez-Buylla, 2002).”
Learning and Survival of Newly Generated Neurons: When Time Matters (2008, methodology): “At first glance, adult neurogenesis seems to have no purpose, because only a subset of newly generated interneurons survive, a substantial proportion of the new cells having only a short existence (Petreanu and Alvarez-Buylla, 2002; Winner et al., 2002; Lagace et al., 2007; Ninkovic et al., 2007).”
Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis (2010, background): “Apoptosis has been observed in the RMS as well as the OB (Petreanu and Alvarez-Buylla, 2002), perhaps representing the early (RMS) and late (OB) critical periods of survival.”
Adult-born neurons facilitate olfactory bulb pattern separation during task engagement (2018, positive): “synaptic plasticity, sensory response pattern, as well as survival rate of ABNs are influenced by olfactory experience during this early period (Alonso et al., 2006; Lemasson et al., 2005; Lepousez et al., 2014; Livneh et al., 2014; Mouret et al., 2008; Petreanu and Alvarez-Buylla, 2002; Quast et al”
A hypothesis about the role of adult neurogenesis in hippocampal function. (2004, background): “The fact that neurogenesis is such a long-lasting process is not unique to the hippocampus, because similar data have been observed for the OB (4, 32).”
Doublecortin expression levels in adult brain reflect neurogenesis (2005, background): “Interestingly, the eliminated supernumerary cells belong mainly to the population of progenitor cells and young neurons (Petreanu & Alvarez-Buylla, 2002; Winner et al., 2002; Dayer et al., 2003).”
Neurogenesis Drives Stimulus Decorrelation in a Model of the Olfactory Bulb (2012, background): “As observed experimentally, reduced odor stimulation leads to a reduction in the size of the granule cell population [15].”
A Critical Time Window for the Recruitment of Bulbar Newborn Neurons by Olfactory Discrimination Learning (2011, background): “, 2 and 7 weeks (Petreanu and Alvarez-Buylla, 2002; Winner et al., 2002; Yamaguchi and Mori, 2005), we report here a decrease in the number of cells between 2 and 5 weeks of age.”