Interactions with the young down-regulate adult olfactory neurogenesis and enhance the maturation of olfactory neuroblasts in sheep mothers

Maïna Brus,Maryse Meurisse,Matthieu Keller,Frédéric Lévy

doi:10.3389/fnbeh.2014.00053

Abstract

New neurons are continuously added in the dentate gyrus (DG) and the olfactory bulb of mammalian brain. While numerous environmental factors controlling survival of newborn neurons have been extensively studied, regulation by social interactions is less documented. We addressed this question by investigating the influence of parturition and interactions with the young on neurogenesis in sheep mothers. Using Bromodeoxyuridine, a marker of cell division, in combination with markers of neuronal maturation, the percentage of neuroblasts and new mature neurons in the olfactory bulb and the DG was compared between groups of parturient ewes which could interact or not with their lamb, and virgins. In addition, a morphological analysis was performed by measuring the dendritic arbor of neuroblasts in both structures. We showed that the postpartum period was associated with a decrease in olfactory and hippocampal adult neurogenesis. In the olfactory bulb, the suppressive effect on neuroblasts was dependent on interactions with the young whereas in the DG the decrease in new mature neurons was associated with parturition. In addition, dendritic length and number of nodes of neuroblasts were significantly enhanced by interactions with the lamb in the olfactory bulb but not in the DG. Because interactions with the young involved learning of the olfactory signature of the lamb, we hypothesize that this learning is associated with a down-regulation in olfactory neurogenesis and an enhancement of olfactory neuroblast maturation. Our assumption is that fewer new neurons decrease cell competition in the olfactory bulb and enhance maturation of those new neurons selected to participate in the learning of the young odor.

Highlights

In most mammals, newborn neurons are continuously provided in two main structures of the brain throughout life, the dentate gyrus (DG) of the hippocampus and the olfactory bulb (Ming and Song, 2005; Curtis et al, 2007; Brus et al, 2013)
Interactions with the young and associated learning, but not parturition, reduce the survival of neuroblasts in the MAIN OLFACTORY BULB (MOB), whereas in the DG, parturition induces a decrease in the number of new neurons
These results suggest that learning of the olfactory signature of the lamb, which occurred during the first mother/young interactions, is associated with a down-regulation in olfactory neurogenesis

Summary

Introduction

Newborn neurons are continuously provided in two main structures of the brain throughout life, the dentate gyrus (DG) of the hippocampus and the olfactory bulb (Ming and Song, 2005; Curtis et al, 2007; Brus et al, 2013). Neural stem cells function as primary precursors in the subventricular zone (SVZ) located on the wall of the lateral ventricles. These cells produce transient amplifying cells which rapidly divide to produce neuroblasts. After reaching the olfactory bulb, the new cells migrate radially and mature into granular interneurons for the majority of them (Rochefort and Lledo, 2005)

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