Olfactory and cortical projections to bulbar and hippocampal adult-born neurons

Abstract

New neurons are continually generated in the subependymal layer of the lateral ventricles and the subgranular zone of dentate gyrus during adulthood. In the subventricular zone, neuroblasts migrate a long distance to the olfactory bulb where they differentiate into granule or periglomerular interneurons. In the hippocampus, neuroblasts migrate a short distance from the subgranular zone to the granule cell layer of the dentate gyrus to become granule neurons. In addition to the short-distance inputs, bulbar interneurons receive long-distance centrifugal afferents from olfactory-recipient structures. Similarly, dentate granule cells receive differential inputs from the medial and lateral entorhinal cortices through the perforant pathway. Little is known concerning these new inputs on the adult-born cells. In this work, we have characterized afferent inputs to 21-day old newly-born neurons. Mice were intraperitoneally injected with bromodeoxyuridine. Two weeks later, rhodamine-labeled dextran-amine was injected into the anterior olfactory nucleus, olfactory tubercle, piriform cortex and lateral and medial entorhinal cortices. One week later, animals were perfused and immunofluorescences were carried out. The data show that projection neurons from the mentioned structures, establish putative synaptic contacts onto 21-day-old neurons in the olfactory bulb and dentate gyrus, in some cases even before they start to express specific subpopulation proteins. Long-distance afferents reach middle and outer one-third portions of the molecular layer of the dentate gyrus and granule and, interestingly, periglomerular layers of the olfactory bulb. In the olfactory bulb, these fibers appear to establish presumptive axo-somatic contacts onto newly-born granule and periglomerular cells.

Somatostatin Serves a Modulatory Role in the Mouse Olfactory Bulb: Neuroanatomical and Behavioral Evidence

“…Stronger retrograde infection by the virus appeared after 5 dpi in extra-olfactory regions, the ventral CA1 of the hippocampus, the claustrum, the paraventricular nucleus of the hypothalamus (not shown), the agranular insular cortex, the basolateral amygdala (BLA) and the locus coeruleus (LC; Figure 8). Except for the LC (Shipley and Ennis, 1996; Schwarz et al, 2015), these regions have not been identified as direct projection areas to the OB (Shipley and Ennis, 1996; Diodato et al, 2016) and the late detection of GFP suggests that they are second- or higher-order projection neurons to the OB (Figure 8), consistent with results using different tracing methods (Shipley and Ennis, 1996; Mohedano-Moriano et al, 2012; De La Rosa-Prieto et al, 2015; Diodato et al, 2016). These data suggest that higher cortical centers modulate SOM signaling in the OB.…”

“…GFP-expressing cells were mainly found in the olfactory cortical area, i.e., the AON, piriform and entorhinal cortex, with rare cells occurring in the dorsal tenia tecta (DTT), and the posteromedial cortical amygdala (PMCo). The number of labeled neurons increased with time in these regions (see Figures 7, 8), which send monosynaptic inputs to the OB (Shipley and Ennis, 1996; Mohedano-Moriano et al, 2012; De La Rosa-Prieto et al, 2015; Diodato et al, 2016). Stronger retrograde infection by the virus appeared after 5 dpi in extra-olfactory regions, the ventral CA1 of the hippocampus, the claustrum, the paraventricular nucleus of the hypothalamus (not shown), the agranular insular cortex, the basolateral amygdala (BLA) and the locus coeruleus (LC; Figure 8).…”

“…Progressively, GFP infected neurons appear in the hypothalamic paraventricular nucleus, claustrum and BLA, suggesting that the virus retrogradely infects second- or third-order neurons. Indeed these regions, except the LC, are not known as direct projection areas to the OB (Shipley and Ennis, 1996; Mohedano-Moriano et al, 2012; De La Rosa-Prieto et al, 2015; Diodato et al, 2016). In conclusion, SOM populations in the mouse OB are tightly contacted by top-down afferents, most of them coming from regions involved in olfactory and emotional processes.…”

Morphine Promotes Astrocyte-Preferential Differentiation of Mouse Hippocampal Progenitor Cells via PKCε-Dependent ERK Activation and TRBP Phosphorylation

“…During adult neurogenesis in the hippocampus, neural progenitor cells (NPCs) in the subgranular zone give rise to neuroblasts and immature neurons, which migrate a short distance into the granule cell layer of the dentate gyrus . The immature or mature neurons differentiated from neuroblast cells and NPCs then integrate into the existing hippocampal circuitry .…”

Analysis of Fos expression in the rat olfactory neurogenic region following single exposure to maternal separation during different neonatal stages

“…The AON is a part of the olfactory cortex and plays a significant role in olfactory signals processing (Illig 2005). Moreover, recent findings revealed its relation also to the adult neurogenesis as the AON is involved in regulation of adult-born interneurons integration in the OB (De La Rosa-Prieto et al 2015).…”