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

Department of Neurobiology, Institute of Life Sciences, Israel.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 05/2012; 32(22):7519-27. DOI: 10.1523/JNEUROSCI.6354-11.2012
Source: PubMed


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.

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    • "In more detail, by injecting a recombinant lentivirus (encoded for synaptophysin, which in turn was fused to green fluorescent protein (GFP)) into the stem cell niche of the SVZ and the rostral migratory stream on GD8, they were able to subsequently image newborn neurons within the OB on PD3 and PD4. This sensitive technique enabled them to reveal two unique properties of adult born granule cells in lactating mothers, namely (1) that they show increased presynaptic density compared with nulliparous mice and (2) that the spines of those neurons born during pregnancy are more stable and undergo enhanced integration into the OB circuitry following parturition (Kopel et al., 2012). "
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    ABSTRACT: The peripartum period represents a time when all mammalian species undergo substantial physiological and behavioural changes, which prepare the female for the demands of motherhood. In addition to behavioural and physiological alterations, numerous brain regions, such as the medial prefrontal cortex, olfactory bulb, medial amygdala and hippocampus are subject to substantial peripartum-associated neuronal, dendritic and synaptic plasticity. These changes, which are temporally- and spatially-distinct are strongly influenced by gonadal and adrenal hormones, such as estrogen and cortisol/corticosterone, which undergo dramatic fluctuations across this period. In this review, we describe our current knowledge regarding these plasticity changes and describe how stress affects such normal adaptations. Finally, we discuss the mechanisms potentially underlying these neuronal, dendritic and synaptic changes and their functional relevance for the mother and her offspring.
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    • "Around gestation day 7, the proliferation reaches a peak in the SVZ/lateral ventricles. After the delivery, the number of new neurons integrated into OB circuits increases, and their dendritic spines exhibit stable features (Shingo et al., 2003; Kopel et al., 2012). These phenomena during early pregnancy and parenting might be important for fine-tuning of olfactory response to mating partners and pups. "
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    • "Bromodeoxyuridine (BrdU), a marker of cell division, was used in combination with two markers of neuronal maturation (doublecortin (DCX), an early maturation marker and NeuN), to compare both hippocampal and olfactory neurogenesis between virgins and parturient ewes which could interact or not with their lamb. In addition, because learning accelerates the maturation of the dendritic trees of newborn neurons in the DG (Tronel et al., 2010; Lemaire et al., 2012), and motherhood is accompanied by changes in the morphology of newborn neurons in the MOB (Kopel et al., 2012), we assessed the influence of lamb olfactory learning on this maturation by measuring the dendritic length and the number of nodes of new neuroblasts. "
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