Abstract
In the olfactory bulb of adult rodents, local interneurons are constantly replaced by immature precursors derived from the subventricular zone. Whether any olfactory sensory process specifically relies on this cell renewal remains largely unclear. By using the well known model of mating-induced imprinting to avoid pregnancy block, which requires accessory olfactory bulb (AOB) function, we demonstrate that this olfactory memory formation critically depends on the presence of newborn granule neurons in this brain region. We show that, in adult female mice, exposure to the male urine compounds involved in mate recognition increases the number of new granule cells surviving in the AOB. This process is modulated by male signals sensed through the vomeronasal organ and, in turn, changes the activity of the downstream amygdaloid and hypothalamic nuclei involved in the pregnancy block response. Chemical depletion of newly generated bulbar interneurons causes strong impairment in mate recognition, thus resulting in a high pregnancy failure rate to familiar mating male odors. Taken together, our results indicate that adult neurogenesis is essential for specific brain functions such as persistent odor learning and mate recognition.
Highlights
Interneurons at the first level of olfactory processing, the main olfactory bulb (MOB), are subjected to life-long replacement (Alvarez-Buylla and Garcia-Verdugo, 2002; Petreanu and AlvarezBuylla, 2002; Gheusi et al, 2009)
We show that adult neurogenesis in the accessory olfactory bulb (AOB) of female mice is regulated by vomeronasal inputs involved in mate pheromonal imprinting: it is enhanced by exposure to male pheromones comprised in the low molecular weight (LMW) fraction of male urine, the same compounds that are critical for mate recognition (Peele et al, 2003; Leinders-Zufall et al, 2004); it is triggered by medial amygdala (MeA) feedback sensory activity, and in turn attenuates the responses to male odors of the AOB–MeA
It is currently unknown at which age the newborn granule cells begin to respond to sensory stimuli and when these neurons are integrated into functional adult AOB circuits
Summary
Interneurons at the first level of olfactory processing, the main olfactory bulb (MOB), are subjected to life-long replacement (Alvarez-Buylla and Garcia-Verdugo, 2002; Petreanu and AlvarezBuylla, 2002; Gheusi et al, 2009). Exposure to male urine odors can facilitate estrous in females, leading to altered pubertyonset, shortened estrous cycle length, and interruption of embryo implantation soon after mating, an effect that is known as selective pregnancy block or Bruce-effect (Bruce, 1966). These neuroendocrine responses are mediated by vomeronasal (VN) excitatory projections to the medial amygdala (MeA), the bed nucleus of the stria terminalis (BNST), the medial hypothalamus (MPA), and the dopaminergic neurons of the arcuate nucleus (arc) that control prolactin release by the anterior pituitary (Li et al, 1989). We hypothesize that the sensorydriven granule cell addition in the AOB may provide the substrate for the pheromonal imprinting on stud male odors in order to avoid pregnancy block
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