Population dynamics of adult‐formed granule neurons of the rat olfactory bulb

Kaplan, Max; McNelly, Nancy A.; Hinds, James W.

doi:10.1002/cne.902390110

Cited by 186 publications

(94 citation statements)

References 22 publications

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“…We also found IGF-II mRNA expressed in the olfactory bulb, as has been observed in chicken and mammals (Ayer-Le Lièvre et al, 1991;Lee et al, 1993). Again, adult neuronal recruitment is well documented in this area (Altman, 1969;Kaplan et al, 1985;Lois and Alvarez-Buylla, 1994) and seems to be regulated by behavior (Corotto et al, 1994). Conversely, no new neurons are added to the cerebellum of adult songbirds, where we detected IGF-II expression, or to the cerebellum of adult rodents (Altman and Bayer, 1993), where IGF-I is expressed and necessary for the acquisition of a simple learning paradigm (Castro-Alamancos and Torres-Aleman, 1994).…”

Section: Functional Implications Of Igf-ii In Other Areas Of the Brainsupporting

confidence: 85%

Selective Expression of Insulin-Like Growth Factor II in the Songbird Brain

et al. 1997

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Neuronal replacement occurs in the forebrain of juvenile and adult songbirds. To address the molecular processes that govern this replacement, we cloned the zebra finch insulin-like growth factor II (IGF-II) cDNA, a factor known to regulate neuronal development and survival in other systems, and examined its expression pattern by in situ hybridization and immunocytochemistry in juvenile and adult songbird brains. The highest levels of IGF-II mRNA expression occurred in three nuclei of the song system: in the high vocal center (HVC), in the medial magnocellular nucleus of the neostriatum (mMAN), which projects to HVC, and to a lesser extent in the robust nucleus of the archistriatum (RA), which receives projections from HVC. IGF-II mRNA expression was developmentally regulated in zebra finches. In canary HVC, monthly changes in IGF-II mRNA expression covaried with previously reported monthly differences in neuron incorporation. Combining retrograde tracers with in situ hybridization and immunocytochemistry, we determined that the HVC neurons that project to area X synthesize the IGF-II mRNA, whereas the adjacent RA-projecting neurons accumulate the IGF-II peptide. Our findings raise the possibility that within HVC IGF-II acts as a paracrine signal between nonreplaceable area X-projecting neurons and replaceable RAprojecting neurons, a mode of action that is compatible with the involvement of IGF-II with the replacement of neurons. Additional roles for IGF-II expression in songbird brain are likely, because expression also occurs in some brain areas outside the song system, among them the cerebellar Purkinje cells in which neurogenesis is not known to occur.

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Section: Functional Implications Of Igf-ii In Other Areas Of the Brainsupporting

confidence: 85%

Selective Expression of Insulin-Like Growth Factor II in the Songbird Brain

et al. 1997

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“…This local proliferation decreases thereafter, becoming insignificant in adults, and leaving the SVZ/RMS production site as the unique source providing neuroblasts during later stages. Previous studies have reported a higher rate of postnatal proliferation in the SVZ compared with the local production within the OB (Hinds, 1968;Altman, 1969;Kaplan et al, 1985;Frazier-Cierpial and Brunjes, 1989), but none have determined the relative contribution between the two sites. Our finding indicates that most postnatally generated neurons are produced at locations caudal to the bulb and subsequently migrate forward.…”

Section: Sites Of Production and Migration Rates Of Newborn Neurons Amentioning

confidence: 95%

Neonatal and Adult Neurogenesis Provide Two Distinct Populations of Newborn Neurons to the Mouse Olfactory Bulb

Lemasson¹

2005

J. Neurosci.

179

159

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In mammals, the olfactory bulb (OB) constitutes one of two regions of the postnatal brain with continuous neurogenesis throughout life. Despite intense explorations of neuronal replacement in the adult OB, little is known about the mechanisms that operate at earlier postnatal stages. This question is particularly pertinent, because the majority of local interneurons are born in the neonate, when olfaction controls vital functions. Here, we analyzed the recruitment of newborn cells to the granule cell (GC) layer (GCL) and found that the postnatal mouse OB is supplied with two spatiotemporally distinct populations of newborn interneurons.Early born [postnatal day 3 (P3) to P7] GCs constitute a threefold larger population compared with those generated later (P14 -P60), and some of them are produced locally within the OB itself. Newborn interneurons generated at P3-P7 were predominantly targeted to the external edge of the GCL, whereas newly generated cells were positioned deeper in older mice. Additionally, although ϳ50% of adult newborn cells were eliminated within a few weeks of reaching the OB, almost the entire population of early born GCs survived until adulthood. Importantly, early olfactory experience specifically modifies the number of newborn GCs in neonates but leaves unaltered the amount of neurons generated during adulthood. Together, these results demonstrate that early postnatal neurogenesis endows the neonate bulbar circuit with newborn GCs that differ morphologically and functionally from those produced in the adult.

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“…In line with this, granule cells, among the key elements for generating LFP oscillations, undergo a permanent renewal (Altman, 1969). Up to 80,000 newborn cells populate the OB per day (Kaplan et al, 1985) (for review, see Peterson, 2002). It would thus be of great interest to evaluate the impact of this neuronal recruitment on odor information processing and to understand how such processing remains constant in a dynamic network.…”

Section: ␥ Oscillations and Olfactory Information Processingmentioning

confidence: 97%

Interplay between Local GABAergic Interneurons and Relay Neurons Generates γ Oscillations in the Rat Olfactory Bulb

Lagier¹,

Carleton²,

Lledo³

2004

J. Neurosci.

241

223

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Olfactory stimuli have been known for a long time to elicit oscillations in olfactory brain areas. In the olfactory bulb (OB), odors trigger synchronous oscillatory activity that is believed to arise from the coherent and rhythmic discharges of large numbers of neurons. These oscillations are known to take part in encoding of sensory information before their transfer to higher subcortical and cortical areas. To characterize the cellular mechanisms underlying ␥ (30 -80 Hz) local field potential (LFP) oscillations, we simultaneously recorded multiunit discharges, intracellular responses, and LFP in rat OB slices. We showed that a single and brief electrical stimulation of olfactory nerve elicited LFP oscillations in the mitral cell body layer lasting Ͼ1 sec. Both action potentials and subthreshold oscillations of mitral/tufted cells, the bulbar output neurons, were precisely synchronized with LFP oscillations. This synchronization arises from the interaction between output neurons and granule cells, the main population of local circuit inhibitory interneurons, through dendrodendritic synapses. Interestingly enough, the synchronization exerted by reciprocal synaptic interactions did not require action potentials initiated in granule cell somata. Finally, local application of a GABA A receptor antagonist at the mitral cell and external plexiform layers confirmed the exclusive role of the granule cell reciprocal synapses in generating the evoked oscillations. We concluded that interneurons located in the granule cell layer generate synaptic activity capable of synchronizing activity of output neurons by interacting with both their subthreshold and spiking activity.

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Population dynamics of adult‐formed granule neurons of the rat olfactory bulb

Cited by 186 publications

References 22 publications

Selective Expression of Insulin-Like Growth Factor II in the Songbird Brain

Selective Expression of Insulin-Like Growth Factor II in the Songbird Brain

Neonatal and Adult Neurogenesis Provide Two Distinct Populations of Newborn Neurons to the Mouse Olfactory Bulb

Interplay between Local GABAergic Interneurons and Relay Neurons Generates γ Oscillations in the Rat Olfactory Bulb

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