Role of Adult-Born Versus Preexisting Neurons Born at P0 in Olfactory Perception in a Complex Olfactory Environment in Mice

Forest, Jérémy; Chalençon, Laura; Midroit, Maëllie; Terrier, Claire; Caillé, Isabelle; Sacquet, Joëlle; Benetollo, Claire; Killian, Martin; Richard, Marion; Didier, Anne; Mandairon, Nathalie

doi:10.1093/cercor/bhz105

Cited by 16 publications

(30 citation statements)

References 52 publications

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“…Previous studies with slice electrophysiology and postmortem histology showed that young abGCs are highly plastic (11,32) and that learning induces spine density increase in abGCs (30,34). Here, our in vivo longitudinal imaging showed that the spine increase in abGCs occurs gradually and cumulatively over days of perceptual learning by increasing new spine formation and decreasing spine elimination.…”

Section: Context Specific Plasticity Of Abgcssupporting

confidence: 56%

“…Together, it appears that adult neurogenesis critically contributes to olfactory perceptual learning to discriminate similar odorants. Studies using postmortem histology have reported that abGCs exhibit learning-and experience-induced increases in apical and basal dendritic spines (18,30). However, in vivo dynamics of abGC plasticity during different behavioral contexts are poorly understood.…”

Section: Introductionmentioning

confidence: 99%

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Context-dependent plasticity of adult-born neurons regulated by cortical feedback

Chen

et al. 2020

Sci. Adv.

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In a complex and dynamic environment, the brain flexibly adjusts its circuits to preferentially process behaviorally relevant information. Here, we investigated how the olfactory bulb copes with this demand by examining the plasticity of adult-born granule cells (abGCs). We found that learning of olfactory discrimination elevates odor responses of young abGCs and increases their apical dendritic spines. This plasticity did not occur in abGCs during passive odor experience nor in resident granule cells (rGCs) during learning. Furthermore, we found that feedback projections from the piriform cortex show elevated activity during learning, and activating piriform feedback elicited stronger excitatory postsynaptic currents in abGCs than rGCs. Inactivation of piriform feedback blocked abGC plasticity during learning, and activation of piriform feedback during passive experience induced learning-like plasticity of abGCs. Our work describes a neural circuit mechanism that uses adult neurogenesis to update a sensory circuit to flexibly adapt to new behavioral demands.

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Section: Context Specific Plasticity Of Abgcssupporting

confidence: 56%

Section: Introductionmentioning

confidence: 99%

Context-dependent plasticity of adult-born neurons regulated by cortical feedback

Chen

et al. 2020

Sci. Adv.

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“…In contrast to the distal GC spines, which primarily make reciprocal dendro-dendritic connections with MC cells, the proximal spines did not have an activity-spine stability relationship with continuous odor exposure. This supports region-specific spine adaptability to differential types of input, as shown in other studies: For distal spines, spine density increased with simple olfactory enrichment 35, 36 and PSD-95 spine density decreased with deprivation, whereas proximal spine density increased 37 . Also, a more complex input, by pairing an odorant with a reward task, caused increased proximal spine density with no effect on distal spines 38 .…”

Section: Discussionsupporting

confidence: 90%

Interneuron activity-structural plasticity association is driven by context-dependent sensory experience

Saha

Meng

Riecke

et al. 2021

Preprint

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Neuronal dendritic spine dynamics provide a plasticity mechanism for altering brain circuit connectivity to integrate new information for learning and memory. Previous in vivo studies in the olfactory bulb (OB) showed that regional increases in activity caused localized spine stability, at a population level, yet how activity affects spine dynamics at an individual neuron level remains unknown. In this study, we tracked in vivo the correlation between an individual neuron’s activity and its dendritic spine dynamics of OB granule cell (GC) interneurons. Odor experience caused a consistent correlation between individual GC activity and spine stability. Dissecting the components of the OB circuit showed that increased principal cell (MC) activity was sufficient to drive this correlation, whereas cell-autonomously driven GC activity had no effect. A mathematical model was able to replicate the GC activity-spine stability correlation and showed MC output having improved odor discriminability while retaining odor memory. These results reveal that GC spine plasticity provides a sufficient network mechanism to decorrelate odors and maintain a memory trace.

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“…In addition to spine plasticity, the olfactory bulb is characterized by substantial neurogenesis of GCs, even in adult animals. Functionally, the adult-born GCs (abGCs) contribute substantially to the animal's ability to learn to discriminate very similar odors, both for perceptual learning [12,41] and for active learning [17]. Many experiments found that the survival of the abGCs depends on their activity [42,43].…”

Section: Discussionmentioning

confidence: 99%

Structural Spine Plasticity in Olfaction: Memory and Forgetting, Enhanced vs. Reduced Discriminability after Learning

Riecke

Meng

2020

Preprint

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How animals learn to discriminate between different sensory stimuli is an intriguing question. An important, common step towards discrimination is the enhancement of differences between the representations of relevant stimuli. This can be part of the learning process. In rodents, the olfac-tory bulb, which is known to contribute to this pattern separation, exhibits extensive structural synaptic plasticity even in adult animals: reciprocal connections between excitatory mitral cells and inhibitory granule cells are persistently formed and eliminated, correlated with mitral cell and granule cell activity. Here we present a Hebbian-type model for this plasticity. It captures the experimental observation that the same learning protocol that enhanced the discriminability of similar stimuli actually reduced that of dissimilar stimuli. The model predicts that the learned bulbar network structure is remembered across training with additional stimuli, unless the new stimuli interfere with the representations of previously learned ones.

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Role of Adult-Born Versus Preexisting Neurons Born at P0 in Olfactory Perception in a Complex Olfactory Environment in Mice

Cited by 16 publications

References 52 publications

Context-dependent plasticity of adult-born neurons regulated by cortical feedback

Context-dependent plasticity of adult-born neurons regulated by cortical feedback

Interneuron activity-structural plasticity association is driven by context-dependent sensory experience

Structural Spine Plasticity in Olfaction: Memory and Forgetting, Enhanced vs. Reduced Discriminability after Learning

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