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Activity-Dependent Extrinsic Regulation of Adult Olfactory Bulb and Hippocampal Neurogenesis Dengke K

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Activity-Dependent Extrinsic Regulation of Adult Olfactory Bulb and Hippocampal Neurogenesis Dengke K INTERNATIONAL SYMPOSIUM ON OLFACTION AND TASTE Activity-dependent Extrinsic Regulation of Adult Olfactory Bulb and Hippocampal Neurogenesis Dengke K. Ma,a,b Woon Ryoung Kim,b,c Guo-li Ming,a,b,c and Hongjun Songa,b,c aThe Solomon Snyder Department of Neuroscience, bInstitute for Cell Engineering, and cDepartment of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA The adult mammalian brain continuously generates new neurons in the olfactory bulb and hippocampus throughout life. Adult neurogenesis, a highly dynamic process, has been shown to be exquisitely modulated by neuronal circuit activity at different stages, from proliferation of adult neural progenitors, to differentiation, maturation, integra- tion, and survival of newborn neurons in the adult brain. Strategic activity-dependent addition of new neurons into the existing neuronal circuitry represents a prominent form of structural plasticity and may contribute to specific brain functions, such as learning, memory, and mood modulation. Here we review extrinsic mechanisms through which adult neurogenesis is regulated by environmental cues, physiological learning-related stimuli, and neuronal activities. Key words: plasticity; adult stem cells; neurotransmitter; neurogenesis; neural activity Introduction dition of populations of new neurons with func- tional synaptic inputs and outputs. Distinct fea- Since the pioneering studies by Altman et al. tures of these two types of plasticity may endow in the early 1960s, adult neurogenesis has now the brain with parallel yet complementary ca- been unambiguously established in discrete pacities for information processing. Common brain regions in most mammals.1–7 New exci- in all neural plasticity and similar to synap- tatory granule neurons and inhibitory granule tic changes, adult neurogenesis is under the and periglomerular interneurons are continu- exquisite control of neural activity. Studies in ously added to existing circuits in the dentate the last few years have delineated the sequen- gyrus and olfactory bulb, respectively (Fig. 1A). tial steps of endogenous adult neurogenesis in Such continuous adult neurogenesis represents these two brain regions, from proliferation and a surprising and intriguing type of plasticity fate specification of adult neural progenitors conserved in adult mammalian brains.5–8 In to differentiation, maturation, axon and den- contrast to the main form of neural plastic- dritic targeting, formation of functional synap- ity, through synaptic-level modification, adult tic inputs and outputs, and selective survival of neurogenesis confers plasticity through the ad- newborn neurons.9,10 Accumulating evidence has implicated adult neurogenesis in specific brain functions, such as olfactory learning, spa- Address for correspondence: Hongjun Song, Ph.D., Institute for tial memory formation, and mediation of be- 11–15 Cell Engineering, Departments of Neurology and Neuroscience, Johns havioral effects of antidepressants. Accord- Hopkins University School of Medicine, 733 N. Broadway, BRB731, Baltimore, MD 21205. Voice: 443-287-7499; fax: 410-614-9568. ingly, many environmental cues, physiological [email protected] learning-related stimuli, and neuronal activities International Symposium on Olfaction and Taste: Ann. N.Y. Acad. Sci. 1170: 664–673 (2009). doi: 10.1111/j.1749-6632.2009.04373.x c 2009 New York Academy of Sciences. 664 Ma et al.: Activity-dependent Adult Neurogenesis 665 Figure 1. Regulation of adult neurogenesis by various types of neural activity. (A) Schematic representation of a sagittal view of the adult mouse brain. New neurons are gener- ated continuously throughout life in the SVZ–olfactory bulb (OB) system and the dentate gyrus (DG) of the hippocampus. (B) Activity-dependent neurogenesis in the adult OB. Transient am- plifying cells give rise to neuroblasts, migrating toward the OB through the rostral migratory stream (RMS). Within the OB, these neuroblasts differentiate into two types of interneurons as the granule cell and periglomerular cell (PGC). Integration into the preexisting circuits by newly entered neurons and their survival are predominantly influenced by odor experiences, such as enriched odor exposure or odor discriminate learning. (C) Activity-dependent neuro- genesis in the dentate gyrus. Neural progenitors in the SGZ proliferate and differentiate into neuroblasts that migrate a short distance into the inner granular cell layer, processes that are modulated by various types of neural activity. The survival and integration of new neurons is also regulated in an activity-dependent manner. (In color in Annals online.) 666 Annals of the New York Academy of Sciences dynamically influence different stages of adult after normal stimulation was restored. Thymi- neurogenesis.16–18 The underlying molecular dine analog labeling revealed that the recov- and cellular mechanisms through which diverse ery was accompanied by the addition of a types of activity selectively regulate different large population of new neurons. Other sim- stages of adult neurogenesis are only beginning ilar experiments have shown that the increased to be unraveled. number of neurons after deprivation is due to rescued survival from the “default” apoptosis program.23–25 Thus, neuronal survival in the Activity-dependent Regulation of olfactory bulb can be profoundly influenced by Adult Olfactory Bulb Neurogenesis afferent activities. Several recent studies have directly exam- New neurons generated in the adult olfac- ined whether physiological exposure to an tory bulb originate from progenitors in the sub- odor-enriched environment or learning tasks ventricular zone (SVZ) of the lateral ventricle affect neurogenesis in the adult olfactory of the forebrain.19 The physical distance be- bulb.26 Using bromodeoxyuridine (BrdU) to tween the place of their birth and place of final birth date progenitors from SVZ and their destination naturally creates two distinct com- progeny, Rochefort et al.27 found that long- partments for potential extrinsic regulation. In term exposure to an odor-enriched environ- the SVZ, adult progenitor cells are located ment dramatically increased the number of in a developmental “vestige” where embry- surviving new neurons at 3 weeks after BrdU onic counterparts generate the majority of neu- injection. The number of BrdU-labeled pro- rons, and not surprisingly their maintenance, genitors was not altered 4 h after a single BrdU proliferation, and fate specification are subject injection, suggesting a lack of effects on cell to numerous developmental signaling controls proliferation. Interestingly, this effect appears in a largely activity-independent manner.19,20 to temporally transient, because the number Highly specialized niche structures, such as a of newborn neurons returned to control levels “glial tunnel,”21 may also function to segregate 30 days after experiencing the odor-enriched the earlier stages of neurogenesis from influ- environment.27 Furthermore, odor discrimina- ences of circuit neuronal activity. After neu- tion learning for an extended period, not just roblasts migrate through the rostral migratory exposure to a single odor, is also able to signifi- stream and reach the bulb, where olfactory cantly increase the survival of newborn neurons information processing takes place, the newly in the olfactory bulb.28 The effects are region generated neurons switch to radial migration to specific, because enriched odor exposure does their final positions and start to receive synap- not influence hippocampal neurogenesis. Al- tic inputs and are subject to activity-dependent though it remains under debate,29,30 olfactory survival and final integration into the preexist- bulb neurogenesis might be associated with spe- ing circuitry. cific olfactory functions, such as olfactory dis- Olfactory bulbs process odorant information crimination and olfactory memory. For exam- from the nose to the brain; thus, the main type ple, olfactory enrichment induces not only an of activity results from sensory stimuli of odor- increase in the number of surviving newborn ant exposure. Using a technique of reversible neurons but also enhancement of short-term ol- olfactory deprivation, Cummings et al. showed factory memory.6,26,27 Conversely,mutant mice that unilateral olfactory deprivation during the deficient in a neural cell adhesion molecule first postnatal month in rodents led to a dra- with reduced olfactory neurogenesis exhibit re- matic reduction in the size of the olfactory bulb duced olfactory sensitivity and olfactory mem- on the experimental side.22 Surprisingly, the ory.11 Studies have also indicated a correlation bulb size had mostly recovered within 40 days between the age-dependent decline of olfactory Ma et al.: Activity-dependent Adult Neurogenesis 667 bulb neurogenesis and fine odorant discrimina- the olfactory bulb. The dentate gyrus receives tion ability.31 These functional correlations sug- inputs from numerous regions of the brain.35 gest that the activities from odorant-related en- Particularly, the SGZ is known to be enriched vironmental stimuli may not only increase the in exuberant neuronal communications be- number of surviving neurons but also enhance tween mature granule neurons and local in- their integration into the circuitry to participate terneurons.36 The spatial proximity to high in information processing. Using immediate- neuronal network circuit activity may place early gene activation to monitor the integra- adult hippocampal neurogenesis under
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