Adult-Born and Preexisting Olfactory Granule Neurons Undergo Distinct Experience-Dependent Modifications of their Olfactory Responses<i>In Vivo</i>

Magavi, Sanjay S. P.; Mitchell, Bartley D.; Szentirmai, Oszkar; Carter, Bob S.; Macklis, Jeffrey D.

doi:10.1523/jneurosci.2250-05.2005

Cited by 192 publications

(185 citation statements)

References 56 publications

Supporting

Mentioning

159

Contrasting

Order By: Relevance

“…Furthermore, newborn neurons respond preferentially to the odorant used for the enrichment. This result is in agreement with a previous study showing that the response of newborn granule cells is altered by olfactory experience in a stimulus-specific manner (13) and further suggests that newborn neurons support the learninginduced improvement of discrimination.…”

Section: Discussionsupporting

confidence: 93%

“…They are formed from neural stem cells located in the subventricular zone (SVZ) of the lateral ventricle (9), and migrate from the SVZ to the OB where they functionally integrate into the neuronal network as granule and periglomerular interneurons (10)(11)(12)(13). Modulation of the rate of newborn neurons formation parallels changes in discrimination induced by sensory experience (14) but the exact role of OB neuronal renewal is still unclear (15).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Olfactory perceptual learning requires adult neurogenesis

Moreno

Linster

Escanilla

et al. 2009

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

231

264

View full text Add to dashboard Cite

Perceptual learning is required for olfactory function to adapt appropriately to changing odor environments. We here show that newborn neurons in the olfactory bulb are not only involved in, but necessary for, olfactory perceptual learning. First, the discrimination of perceptually similar odorants improves in mice after repeated exposure to the odorants. Second, this improved discrimination is accompanied by an elevated survival rate of newborn inhibitory neurons, preferentially involved in processing of the learned odor, within the olfactory bulb. Finally, blocking neurogenesis before and during the odorant exposure period prevents this learned improvement in discrimination. Olfactory perceptual learning is thus mediated by the reinforcement of functional inhibition in the olfactory bulb by adult neurogenesis. discrimination ͉ mice ͉ enrichment ͉ olfactory bulb P erceptual learning is an implicit (nonassociative) form of learning in which discrimination between sensory stimuli is improved by previous experience (1). For instance, animals trained on a tactile discrimination task improve their behavioral performances and in parallel, the neural representation of the stimuli is sharpened (2, 3). In the olfactory modality, perceptual learning has been shown to occur in humans (4), and an experimental model of olfactory perceptual learning has recently been proposed in rats (5). Olfactory perceptual learning is crucial for basic olfactory functions because it sets the degree of discrimination between stimuli, and thus contributes to the perceptual representation of the environment, which guides the animal's behavior. However, neural mechanisms underlying such changes of perception remain elusive. We here show that a modulation of newborn cell survival in the olfactory bulb (OB) underlies olfactory perceptual learning. We show that neurogenesis is not only involved in, but necessary for perceptual learning to occur.We have shown that odor enrichment enhances rats' ability to discriminate between chemically similar odorants in a relatively odor-unspecific manner (5, 6). Indeed, the discrimination of a pair of similar odorants is improved by enrichment with the same odorants or with other odorants that activate regions of the OB partially overlapping with the regions activated by the discriminated pair. Even if the mechanisms underlying this learning remain unclear, it has been shown that infusions of NMDA into the OB improves odor discrimination in a manner similar to odor enrichment indicating that changes in OB processing contribute at least partially to the perceptual plasticity (5). A computational model proposed that activation of OB neurons produces widespread changes in inhibitory processing, which can underlie the observed improvement of odor discrimination (5). In support to this model, odor exposure has been shown to increase inhibition of mitral cells (7) and to increase the responsiveness of the inhibitory granule cells to odorants, as measured by expression of an immediate early gene (8).Inhibitory neuro...

show abstract

Section: Discussionsupporting

confidence: 93%

mentioning

confidence: 99%

Olfactory perceptual learning requires adult neurogenesis

Moreno

Linster

Escanilla

et al. 2009

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

231

264

View full text Add to dashboard Cite

show abstract

“…Adult neurogenesis is the birth of new neurons, which continues postnatally and into adulthood in the brains of several mammalian species, including humans. New cells integrate into hippocampal and olfactory circuits, leading to enhanced synaptic plasticity (Nissant et al, 2009), increased responsiveness to stimuli (Magavi et al, 2005), and improved learning and memory processes (Shors et al, 2001;Snyder et al, 2005;Winocur et al, 2006;Deng et al, 2009;Rochefort et al, 2002;Sultan et al, 2010).…”

mentioning

confidence: 99%

Social regulation of adult neurogenesis in a eusocial mammal

et al. 2014

View full text Add to dashboard Cite

The present study examined social status and adult neurogenesis in the naked mole rat. These animals live in large colonies with a strict reproductive dominance hierarchy; one female and 1-3 males breed, while other members are subordinate and reproductively suppressed. We examined whether social status affects doublecortin (DCX; a marker for immature neurons) immunoreactivity in the dentate gyrus, piriform cortex (PCx), and basolateral amygdala (BLA) by comparing breeders to subordinates. We also examined subordinates removed from their colony and paired with opposite-or same-sex conspecifics for 6 months. Breeders had reduced DCX immunoreactivity in all areas, with BLA effects confined to females. Effects of housing condition were region-specific, with higher PCx DCX immunoreactivity observed in oppositethan same-sex paired subordinates regardless of gonadal status. The opposite pattern was observed in the BLA. Future work will clarify whether findings are attributable to status differences in stress, behavioural plasticity, or life stage.iii

show abstract

“…wt and GluN2B fl/fl mice were stereotactically injected with a retrovirus mix (MolR:GFP:2a:Cre and MolR:mCherry). At 17 d.p.i., IEG (c-Fos) response of GCs was assessed in mice that had no previous experience with the test odors (essentially following the procedure described by Magavi et al, 2005). Mice were housed individually in microisolator cages receiving 12 L/min of humidified, HEPA-filtered air for 24 h to reduce background activity.…”

Section: ) Psd-95gfpmentioning

confidence: 99%

GluN2B-Containing NMDA Receptors Promote Wiring of Adult-Born Neurons into Olfactory Bulb Circuits

Kelsch

Eliava

et al. 2012

J. Neurosci.

View full text Add to dashboard Cite

In the developing telencephalon, NMDA receptors (NMDARs) are composed of GluN1 and GluN2B subunits. These "young" NMDARs set a brake on synapse recruitment in neurons of the neonatal cortex. The functional role of GluN2B for synapse maturation of adult-born granule cells (GCs) in the olfactory bulb has not been established and may differ from that of differentiating neurons in immature brain circuits with sparse activity. We genetically targeted GCs by sparse retroviral delivery in mouse subventricular zone that allows functional analysis of single genetically modified cells in an otherwise intact environment. GluN2B-deficient GCs did not exhibit impairment with respect to the first developmental milestones such as synaptogenesis, dendrite formation, and maturation of inhibitory synaptic inputs. However, GluN2B deletion prevented maturation of glutamatergic synaptic input. This severe impairment in synaptic development was associated with a decreased response to novel odors and eventually led to the demise of adult-born GCs. The effect of GluN2B on GC survival is subunit specific, since it cannot be rescued by GluN2A, the subunit dominating mature NMDAR function. Our observations indicate that, GluN2B-containing NMDARs promote synapse activation in adult-born GCs that integrate in circuits with high and correlated synaptic activity. The function of GluN2B-containing NMDARs on synapse maturation can thus be bidirectional depending on the environment.

show abstract

Adult-Born and Preexisting Olfactory Granule Neurons Undergo Distinct Experience-Dependent Modifications of their Olfactory ResponsesIn Vivo

Cited by 192 publications

References 56 publications

Olfactory perceptual learning requires adult neurogenesis

Olfactory perceptual learning requires adult neurogenesis

Social regulation of adult neurogenesis in a eusocial mammal

GluN2B-Containing NMDA Receptors Promote Wiring of Adult-Born Neurons into Olfactory Bulb Circuits

Contact Info

Product

Resources

About