Sensory Input Regulates Spatial and Subtype-Specific Patterns of Neuronal Turnover in the Adult Olfactory Bulb

Sawada, Masato; Kaneko, Naoko; Inada, Hiroyuki; Wake, Hiroaki; Kato, Yasuko; Yanagawa, Yuchio; Kobayashi, Kazuto; Nemoto, Tomomi; Nabekura, Junichi; Sawamoto, Kazunobu

doi:10.1523/jneurosci.0614-11.2011

Cited by 75 publications

(109 citation statements)

References 50 publications

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“…Second, minocycline treatment does not change the amount of neuroblasts reaching the OB, indicating that minocycline does not affect the SVZ production of neuroblasts. This finding extends previous results showing that odorant deprivation, or olfactory deafferentation, leads to a decreased survival of new OB neurons (Corotto et al, 1994;Petreanu and Alvarez-Buylla, 2002;Yamaguchi and Mori, 2005;Mandairon et al, 2006;Bastien-Dionne et al, 2010;Sawada et al, 2011). From the present study, we conclude that activated microglia is a key regulator capable of adjusting the survival of maturing adultborn OB neurons, at least following chemical lesion of the sensory afferents.…”

Section: Tuning the Survival Of Adult-born Neurons During Ob Inflammasupporting

confidence: 92%

“…3C). Together, these findings support previous studies showing that sensory deprivation, or olfactory deafferentation, reduces adult OB neurogenesis by decreasing the survival of newly generated neurons (Corotto et al, 1994;Fiske and Brunjes, 2001;Petreanu and AlvarezBuylla, 2002;Yamaguchi and Mori, 2005;Mandairon et al, 2006;Bastien-Dionne et al, 2010;Sawada et al, 2011).…”

Section: The Survival Of New Neurons Decreases After Sensory Deafferesupporting

confidence: 90%

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Early Activation of Microglia Triggers Long-Lasting Impairment of Adult Neurogenesis in the Olfactory Bulb

Lazarini

Gabellec²,

Torquet³

et al. 2012

J. Neurosci.

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Microglia, the innate immune cells of the brain, engulf and eliminate cellular debris during brain injury and disease. Recent observations have extended their roles to the healthy brain, but the functional impact of activated microglia on neural plasticity has so far been elusive. To explore this issue, we investigated the role of microglia in the function of the adult olfactory bulb network in which both sensory afferents and local microcircuits are continuously molded by the arrival of adult-born neurons. We show here that the adult olfactory bulb hosts a large population of resident microglial cells. Deafferentation of the olfactory bulb resulted in a transient activation of microglia and a concomitant reduction of adult olfactory bulb neurogenesis. One day after sensory deafferentation, microglial cells proliferate in the olfactory bulb, and their numbers peaked at day 3, and reversed at day 7 after lesion. Similar lesions performed on immunodeficient mice demonstrate that the both innate and adaptive lymphocyte responses are dispensable for the lesion-induced microglial proliferation and activation. In contrast, when mice were treated with an antiinflammatory drug to prevent microglial activation, olfactory deafferentation did not reduce adult neurogenesis, showing that activated microglial cells per se, and not the lack of sensory experience, relates to the survival of adult-born neurons. We conclude that the status of the resident microglia in the olfactory bulb is an important factor directly regulating the survival of immature adult-born neurons.

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Section: Tuning the Survival Of Adult-born Neurons During Ob Inflammasupporting

confidence: 92%

Section: The Survival Of New Neurons Decreases After Sensory Deafferesupporting

confidence: 90%

Early Activation of Microglia Triggers Long-Lasting Impairment of Adult Neurogenesis in the Olfactory Bulb

Lazarini

Gabellec²,

Torquet³

et al. 2012

J. Neurosci.

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“…Neurotransmission between pre-and postsynaptic fibers in the GL of the OB is extensively modulated by periglomerular interneurons that exclusively express tyrosine TH, CB, or calretinin (CR) (19). Deprivation of presynaptic input from the ONL in rodents, either by treatment with zinc sulfate or by naris occlusion, was previously shown to reduce both TH expression and dopamine levels in the GL of the OB (20,21), whereas naris reopening resulted in the generation of new TH + interneurons (22). We therefore expected that the reduced thickness of the ONL in the OB of Gnao −/− mice would be associated with a reduction in TH expression or a reduced number of TH + periglomerular cells.…”

Section: Resultsmentioning

confidence: 99%

Development of the main olfactory system and main olfactory epithelium-dependent male mating behavior are altered in G _o -deficient mice

Choi

Kim

Choi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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In mammals, initial detection of olfactory stimuli is mediated by sensory neurons in the main olfactory epithelium (MOE) and the vomeronasal organ (VNO). The heterotrimeric GTP-binding protein G o is widely expressed in the MOE and VNO of mice. Early studies indicated that G o expression in VNO sensory neurons is critical for directing social and sexual behaviors in female mice [Oboti L, et al. (2014) BMC Biol 12:31]. However, the physiological functions of G o in the MOE have remained poorly defined. Here, we examined the role of G o in the MOE using mice lacking the α subunit of G o . Development of the olfactory bulb (OB) was perturbed in mutant mice as a result of reduced neurogenesis and increased cell death. The balance between cell types of OB interneurons was altered in mutant mice, with an increase in the number of tyrosine hydroxylase-positive interneurons at the expense of calbindin-positive interneurons. Sexual behavior toward female mice and preference for female urine odors by olfactory sensory neurons in the MOE were abolished in mutant male mice. Our data suggest that G o signaling is essential for the structural and functional integrity of the MOE and for specification of OB interneurons, which in turn are required for the transmission of pheromone signals and the initiation of mating behavior with the opposite sex.heterotrimeric G o protein | olfactory mucosa | olfactory bulb interneuron | tyrosine monooxygenase | sexual behavior P heromones evoke diverse social and sexual behaviors in animals of the same species. In mammals, initial detection of olfactory stimuli is mediated by sensory neurons in the main olfactory epithelium (MOE) and vomeronasal organ (VNO). Early studies indicated that the VNO is largely responsible for the detection of pheromones and the consequent direction of social and sexual behaviors (1). VNO sensory neurons (VSNs) express distinct types of vomeronasal receptors: type 1 (V1Rs) in the apical region and type 2 (V2Rs) in the basal region. These receptors couple, respectively, to G i and G o members of the heterotrimeric GTPbinding protein family. It has been suggested that, following ligand binding to V1Rs and V2Rs, the Gβγ subunits released from G i and G o activate phospholipase C and increase the intracellular concentration of Ca 2+ . Ca 2+ ions induce opening of small Ca 2+ -activated K + (SK3) channels, subsequently activating Ca 2+ -activated Cl − channels (CACCs). In the VNO, Gβγ can also directly induce the opening of G protein-activated inward rectifying K + (GIRK) channels independently of transient receptor potential cation channel C2 (TRPC2) (2). Because of the VNO's high luminal K + concentration (2), opening of SK3 and GIRK channels leads to depolarization of VSNs and transmission of pheromone signals. Targeted deletion of the TRPC2 gene abrogates gender identification and intermale aggression without affecting male-to-female mating behavior in male mice (3, 4). Targeted deletion of the GIRK1 gene partially attenuates mating behavior of the male toward fem...

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“…4A), we showed that, in live animals, the addition and elimination of periglomerular cells are dynamically controlled by olfactory input in a neuronal subtype-specific manner. 94 To examine the spatiotemporal relationship between lost and replaced neurons, we developed a method for in vivo two-photon laser-ablation of periglomerular cells (Fig. 4B), by which we could selectively eliminate targeted neurons in live animals.…”

Section: Neuronal Maturation and Turnover In The Olfactory Bulbmentioning

confidence: 99%

“…95 Thus, it is possible that adult-born olfactory interneurons show subtype-specific turnover patterns. 94 The turnover of olfactory interneurons is thought to be important for both the maintenance and the plasticity of olfactory functions. Further analysis of the spatiotemporal regulation of neuronal turnover will be needed to understand how neuronal turnover contributes to structural and functional plasticity and/or stability in the adult OB.…”

Section: Neuronal Maturation and Turnover In The Olfactory Bulbmentioning

confidence: 99%

Mechanisms of Neurogenesis in the Normal and Injured Adult Brain

Sawada

Sawamoto

2013

Keio J. Med.

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Even in the adult brain, new neurons are continuously generated from endogenous neural stem cells that reside in two restricted regions: the subventricular zone (SVZ) of the lateral ventricle and the dentate gyrus of the hippocampus. These new neurons are integrated into the mature neuronal circuitry and become involved in various functions, thereby contributing to structural and functional plasticity in the adult brain. In this review, we summarize our recent findings on the regulatory mechanisms of SVZ neurogenesis under physiological and pathological conditions in various animal models. Some of these findings were presented in the Kitazato Prize Lecture at Keio University School of Medicine in

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Sensory Input Regulates Spatial and Subtype-Specific Patterns of Neuronal Turnover in the Adult Olfactory Bulb

Cited by 75 publications

References 50 publications

Early Activation of Microglia Triggers Long-Lasting Impairment of Adult Neurogenesis in the Olfactory Bulb

Early Activation of Microglia Triggers Long-Lasting Impairment of Adult Neurogenesis in the Olfactory Bulb

Development of the main olfactory system and main olfactory epithelium-dependent male mating behavior are altered in G _o -deficient mice

Mechanisms of Neurogenesis in the Normal and Injured Adult Brain

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Sensory Input Regulates Spatial and Subtype-Specific Patterns of Neuronal Turnover in the Adult Olfactory Bulb

Cited by 75 publications

References 50 publications

Early Activation of Microglia Triggers Long-Lasting Impairment of Adult Neurogenesis in the Olfactory Bulb

Early Activation of Microglia Triggers Long-Lasting Impairment of Adult Neurogenesis in the Olfactory Bulb

Development of the main olfactory system and main olfactory epithelium-dependent male mating behavior are altered in G o -deficient mice

Mechanisms of Neurogenesis in the Normal and Injured Adult Brain

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Product

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Development of the main olfactory system and main olfactory epithelium-dependent male mating behavior are altered in G _o -deficient mice