Enhanced Synaptic Integration of Adult-Born Neurons in the Olfactory Bulb of Lactating Mothers

Abstract

One of the most dramatic events during the life of adult mammals is the transition into motherhood. This transition is accompanied by specific maternal behaviors, displayed by the mother, that ensure the survival and the well-being of her offspring. The execution of these behaviors is most likely accompanied by plastic changes in specific neuronal circuits, but these are still poorly defined. In this work, we studied the mammalian olfactory bulb (OB), which has been shown to be an essential brain region for maternal behaviors in mice. In the OB, we focused on adult-born neurons, which are continuously incorporated into the circuit during adulthood, thus providing a potential substrate for heightened plasticity after parturition. We analyzed the dynamics and morphological characteristics of adult-born granule cells (abGCs), innervating the OB of primiparous lactating mothers, shortly after parturition as well as in naive females. In vivo time-lapse imaging of abGCs revealed that dendritic spines were significantly more stable in lactating mothers compared with naive virgins. In contrast, spine stability of resident GCs remained unchanged after parturition. In addition, while spine size distribution of abGCs was approximately similar between mothers and naive virgins, the spine density of abGCs was lower in lactating mothers and the density of their presynaptic components was higher. These structural features are indicative of enhanced integration of adult-born neurons into the bulbar circuitry of lactating mothers. This enhanced integration may serve as a cellular mechanism, supporting changes in olfactory coding of new mothers during their first days following parturition.

Chemical olfactory signals and parenthood in mammals

“…Compared to virgins, lactating mothers showed an increase in synaptophysin along their dendritic tree, associated with decreased spine dynamics and spine densities. This increase was specific to newborn cells in the MOB, and was not observed in the resident granular cells (Kopel et al, 2012). Whether the enhanced maturation of newborn olfactory neurons could be a direct consequence of exposure to pup odors and/or of learning these odors remains to be investigated.…”

Integrating Hebbian and homeostatic plasticity: the current state of the field and future research directions

“…Hebbian mechanisms have correlates in synaptic structural plasticity, in which LTP is correlated with the formation of new spines [71,72], and LTD is associated with the loss of pre-existing spines [73]. The in vivo upregulation of spine dynamics has been observed following sensory deprivation in somatosensory cortex [74 -77], olfactory cortex [78,79], auditory cortex [80] and visual cortex [74,77,81 -83], and following learning in motor cortex [84][85][86] where the memory of the learned motor task depends on the newly formed synapses [87].…”

Neural control of maternal and paternal behaviors

“…Moreover, a significant modulation of sound-evoked responses by pup odors has been shown in the primary auditory cortex of lactating female mice shortly after parturition, with neurons from lactating mothers displaying more sensitivity to sounds than virgins (44). In the olfactory system, mitral cells in the olfactory bulb of female ewes have been shown to undergo marked changes in sensory responses to lamb versus food odors after parturition (46, 47). Moreover, in vivo time-lapse imaging of adult newly born granule cells in mice showed an enhanced integration of these neurons into the olfactory circuit of lactating mothers (46).…”