Abstract
The integration of newly generated neurons persists throughout life in the mammalian olfactory bulb and hippocampus, regions involved in olfactory and spatial learning. Social cues can be potent stimuli for increasing adult neurogenesis; for example, odors from dominant but not subordinate male mice increase neurogenesis in both brain regions of adult females. However, little is known about the role of neurogenesis in social recognition or the assessment of potential mates. Dominant male mice scent-mark territories using urine that contains a number of pheromones including darcin (MUP20), a male-specific major urinary protein that stimulates rapid learned attraction to the spatial location and individual odor signature of the scent owner. Here we investigate whether exposure to darcin stimulates neurogenesis in the female brain. Hippocampal neurons and cellular proliferation in the lateral ventricles that supply neurons to the olfactory bulbs increased in females exposed for 7 days to male urine containing at least 0.5 μg/μl darcin. Darcin was effective whether presented alone or in the context of male urine, but other information in male urine appeared to modulate the proliferative response. When exposed to urine from wild male mice, hippocampal proliferation increased only if urine was from the same individual over 7 days, suggesting that consistency of individual scent signatures is important. While 7 days exposure to male scent initiated the first stages of increased neurogenesis, this caused no immediate increase in female attraction to the scent or in the strength or robustness of spatial learning in short-term conditioned place preference tests. The reliable and consistent stimulation of neurogenesis by a pheromone important in rapid social learning suggests that this may provide an excellent model to explore the relationship between the integration of new neurons and plasticity in spatial and olfactory learning in a socially-relevant context.
Highlights
Neurogenesis, or the generation and integration of new neurons, persists throughout life primarily in two structures of the adult mammalian brain: the olfactory bulb and the hippocampus.Pheromonal stimulation of neurogenesis in female miceThe precise impact of this plasticity on function in these different regions remains elusive, but neurogenesis has been implicated in a range of learning tasks including conditioned learning, memory consolidation and odor discrimination (Gould et al, 1999; Deng et al, 2010; Kageyama et al, 2012)
New neurons added to the olfactory bulbs in adulthood are generated within the sub-ventricular zone (SVZ), the cellular layer found within the walls of the lateral ventricles in the forebrain (Luskin, 1993; Lledo and Saghatelyan, 2005)
To establish (a) whether the components of male odors that stimulate this increase are located in urine, which competitive adult male mice use to scent mark their territories; and (b) whether increased neurogenesis depends on the presence of the sex pheromone darcin in male urine, we used females of the CD-1 strain in which Mak et al (2007) had originally demonstrated the effect of prolonged exposure to male scent on female neurogenesis
Summary
The precise impact of this plasticity on function in these different regions remains elusive, but neurogenesis has been implicated in a range of learning tasks including conditioned learning, memory consolidation and odor discrimination (Gould et al, 1999; Deng et al, 2010; Kageyama et al, 2012) It may be a potential mediator of the essential balance between circuit stability and plasticity (reviewed by Lledo et al, 2006). Continual production of neurons throughout life requires that this region contain a large population of neural stem cells; approximately 30,000 new cells, or neuroblasts, are produced daily within the mouse SVZ (Lois and Alvarez-Buylla, 1994) These newly generated cells must migrate to the mature bulbar networks (Lois and Alvarez-Buylla, 1994), joining the rostral migratory stream in chains where blood vessels provide anchorage (Lois and Alvarez-Buylla, 1994; Whitman et al, 2009). The initial stages of proliferation and migration take approximately 7 days; cells have a mature neuronal morphology and are integrated into existing olfactory bulb circuits by day 30 (reviewed by Abrous et al, 2005), staying functional for up to a year (Winner et al, 2002)
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