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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    • "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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    ABSTRACT: The olfactory bulb (OB) is the first central processing center for olfactory information connecting with higher areas in the brain, and this neuronal circuitry mediates a variety of odor-evoked behavioral responses. In the adult mammalian brain, continuous neurogenesis occurs in two restricted regions, the subventricular zone (SVZ) of the lateral ventricle and the hippocampal dentate gyrus. New neurons born in the SVZ migrate through the rostral migratory stream and are integrated into the neuronal circuits of the OB throughout life. The significance of this continuous supply of new neurons in the OB has been implicated in plasticity and memory regulation. Two decades of huge investigation in adult neurogenesis revealed the biological importance of integration of new neurons into the olfactory circuits. In this review, we highlight the recent findings about the physiological functions of newly generated neurons in rodent OB circuits and then discuss the contribution of neurogenesis in the brain function. Finally, we introduce cutting edge technologies to monitor and manipulate the activity of new neurons.
    Frontiers in Neuroscience 05/2014; 8(8):121. DOI:10.3389/fnins.2014.00121 · 3.66 Impact Factor
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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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    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.
    Frontiers in Behavioral Neuroscience 02/2014; 8:53. DOI:10.3389/fnbeh.2014.00053 · 3.27 Impact Factor
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    • "Animal care and experiments were approved by the Hebrew University Animal Care and Use Committee. To label adult-born neurons, we injected a lentivirus encoding either GFP (for targeted recordings) or Syp-GFP (for labeling putative presynapses; Kelsch et al., 2008; Kopel et al., 2012) into the RMS, as described previously (Bardy et al., 2010; Livneh and Mizrahi, 2012; Nissant et al., 2009). See Supplemental Experimental Procedures for further details. "
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    ABSTRACT: The adult mammalian brain is continuously supplied with adult-born neurons in the olfactory bulb (OB) and hippocampus, where they are thought to be important for circuit coding and plasticity. However, direct evidence for the actual involvement of these neurons in neural processing is still lacking. We recorded the spiking activity of adult-born periglomerular neurons in the mouse OB in vivo using two-photon-targeted patch recordings. We show that odor responsiveness reaches a peak during neuronal development and then recedes at maturity. Sensory enrichment during development enhances the selectivity of adult-born neurons after maturation, without affecting neighboring resident neurons. Thus, in the OB circuit, adult-born neurons functionally integrate into the circuit, where they acquire distinct response profiles in an experience-dependent manner. The constant flow of these sensitive neurons into the circuit provides it with a mechanism of long-term plasticity, wherein new neurons mature to process odor information based on past demands.
    Neuron 02/2014; 81(5). DOI:10.1016/j.neuron.2014.01.007 · 15.05 Impact Factor
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