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Consolidation of an olfactory memory trace in the olfactory bulb is required for learning-induced survival of adult-born neurons and long-term memory.

Kermen F, Sultan S, Sacquet J, Mandairon N, Didier A - PLoS ONE (2010)

Bottom Line: We addressed this question by investigating the effect of bulbar consolidation of olfactory learning on memory and neurogenesis.Subsequently, we used a pharmacological approach to block consolidation in the olfactory bulb, consisting in intrabulbar infusion of the protein synthesis inhibitor anisomycin, and found impaired learning and no increase in neurogenesis, while basic olfactory processing and the basal rate of adult-born neuron survival remained unaffected.We can thus propose a model in which consolidation processes in the olfactory bulb determine both survival of adult-born neurons and long-term olfactory memory.

View Article: PubMed Central - PubMed

Affiliation: Université Lyon 1, Centre National de la Recherche Scientifique, UMR 5020 Neurosciences Sensorielles, Comportement, Cognition, Lyon, France. fkermen@olfac.univ-lyon1.fr

ABSTRACT

Background: It has recently been proposed that adult-born neurons in the olfactory bulb, whose survival is modulated by learning, support long-term olfactory memory. However, the mechanism used to select which adult-born neurons following learning will participate in the long-term retention of olfactory information is unknown. We addressed this question by investigating the effect of bulbar consolidation of olfactory learning on memory and neurogenesis.

Methodology/principal findings: Initially, we used a behavioral ecological approach using adult mice to assess the impact of consolidation on neurogenesis. Using learning paradigms in which consolidation time was varied, we showed that a spaced (across days), but not a massed (within day), learning paradigm increased survival of adult-born neurons and allowed long-term retention of the task. Subsequently, we used a pharmacological approach to block consolidation in the olfactory bulb, consisting in intrabulbar infusion of the protein synthesis inhibitor anisomycin, and found impaired learning and no increase in neurogenesis, while basic olfactory processing and the basal rate of adult-born neuron survival remained unaffected. Taken together these data indicate that survival of adult-born neurons during learning depends on consolidation processes taking place in the olfactory bulb.

Conclusion/significance: We can thus propose a model in which consolidation processes in the olfactory bulb determine both survival of adult-born neurons and long-term olfactory memory. The finding that adult-born neuron survival during olfactory learning is governed by consolidation in the olfactory bulb strongly argues in favor of a role for bulbar adult-born neurons in supporting olfactory memory.

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Neuronal differentiation in conditioned (C), pseudo-conditioned (PC) and naive animals.A. Representative BrdU/NeuN double-labeled cell with orthogonal views. B. No difference in percentage of double-labeled cells was found between spaced and massed trained animals (group effect, F(3,8) = 0.231, p = 0.87) (Bi), nor between saline and anisomycin injected animals (group effect, F(3,5) = 0.512, p = 0.69) (Bii).
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pone-0012118-g002: Neuronal differentiation in conditioned (C), pseudo-conditioned (PC) and naive animals.A. Representative BrdU/NeuN double-labeled cell with orthogonal views. B. No difference in percentage of double-labeled cells was found between spaced and massed trained animals (group effect, F(3,8) = 0.231, p = 0.87) (Bi), nor between saline and anisomycin injected animals (group effect, F(3,5) = 0.512, p = 0.69) (Bii).

Mentions: We then looked at the effect of these two different learning paradigms on the rate of neurogenesis in the OB, known to be affected by learning [26], [28]. Due to the Bromodeoxyurine (BrdU) injection protocol, changes in the rate of neurogenesis will reflect modulation of the adult-born cell survival. The density of newborn cells (Figure 1Ci) was then assessed in the granule cell layer of both groups (see Methods). Following spaced conditioning, the density of newborn cells was increased compared to that of the pseudo-conditioned animals (p<0.05) (Figure 1Cii). Interestingly, the massed conditioning did not modulate neurogenesis; the level of newborn cells was similar in the conditioned and pseudo-conditioned animals (p>0.05) (Figure 1Ciii). The difference in BrdU-positive cell density in the massed versus spaced groups is due to the difference in the number of BrdU injections (see Methods). The percentage of BrdU-positive cells expressing the neuronal marker NeuN (≈85%) was similar in all groups (Figure 2A, Bi). These data indicate that the 24-hour time interval was necessary to allow a learning-induced increase in neurogenesis and thus that newborn neuron survival may be related to memory consolidation processes.


Consolidation of an olfactory memory trace in the olfactory bulb is required for learning-induced survival of adult-born neurons and long-term memory.

Kermen F, Sultan S, Sacquet J, Mandairon N, Didier A - PLoS ONE (2010)

Neuronal differentiation in conditioned (C), pseudo-conditioned (PC) and naive animals.A. Representative BrdU/NeuN double-labeled cell with orthogonal views. B. No difference in percentage of double-labeled cells was found between spaced and massed trained animals (group effect, F(3,8) = 0.231, p = 0.87) (Bi), nor between saline and anisomycin injected animals (group effect, F(3,5) = 0.512, p = 0.69) (Bii).
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2921340&req=5

pone-0012118-g002: Neuronal differentiation in conditioned (C), pseudo-conditioned (PC) and naive animals.A. Representative BrdU/NeuN double-labeled cell with orthogonal views. B. No difference in percentage of double-labeled cells was found between spaced and massed trained animals (group effect, F(3,8) = 0.231, p = 0.87) (Bi), nor between saline and anisomycin injected animals (group effect, F(3,5) = 0.512, p = 0.69) (Bii).
Mentions: We then looked at the effect of these two different learning paradigms on the rate of neurogenesis in the OB, known to be affected by learning [26], [28]. Due to the Bromodeoxyurine (BrdU) injection protocol, changes in the rate of neurogenesis will reflect modulation of the adult-born cell survival. The density of newborn cells (Figure 1Ci) was then assessed in the granule cell layer of both groups (see Methods). Following spaced conditioning, the density of newborn cells was increased compared to that of the pseudo-conditioned animals (p<0.05) (Figure 1Cii). Interestingly, the massed conditioning did not modulate neurogenesis; the level of newborn cells was similar in the conditioned and pseudo-conditioned animals (p>0.05) (Figure 1Ciii). The difference in BrdU-positive cell density in the massed versus spaced groups is due to the difference in the number of BrdU injections (see Methods). The percentage of BrdU-positive cells expressing the neuronal marker NeuN (≈85%) was similar in all groups (Figure 2A, Bi). These data indicate that the 24-hour time interval was necessary to allow a learning-induced increase in neurogenesis and thus that newborn neuron survival may be related to memory consolidation processes.

Bottom Line: We addressed this question by investigating the effect of bulbar consolidation of olfactory learning on memory and neurogenesis.Subsequently, we used a pharmacological approach to block consolidation in the olfactory bulb, consisting in intrabulbar infusion of the protein synthesis inhibitor anisomycin, and found impaired learning and no increase in neurogenesis, while basic olfactory processing and the basal rate of adult-born neuron survival remained unaffected.We can thus propose a model in which consolidation processes in the olfactory bulb determine both survival of adult-born neurons and long-term olfactory memory.

View Article: PubMed Central - PubMed

Affiliation: Université Lyon 1, Centre National de la Recherche Scientifique, UMR 5020 Neurosciences Sensorielles, Comportement, Cognition, Lyon, France. fkermen@olfac.univ-lyon1.fr

ABSTRACT

Background: It has recently been proposed that adult-born neurons in the olfactory bulb, whose survival is modulated by learning, support long-term olfactory memory. However, the mechanism used to select which adult-born neurons following learning will participate in the long-term retention of olfactory information is unknown. We addressed this question by investigating the effect of bulbar consolidation of olfactory learning on memory and neurogenesis.

Methodology/principal findings: Initially, we used a behavioral ecological approach using adult mice to assess the impact of consolidation on neurogenesis. Using learning paradigms in which consolidation time was varied, we showed that a spaced (across days), but not a massed (within day), learning paradigm increased survival of adult-born neurons and allowed long-term retention of the task. Subsequently, we used a pharmacological approach to block consolidation in the olfactory bulb, consisting in intrabulbar infusion of the protein synthesis inhibitor anisomycin, and found impaired learning and no increase in neurogenesis, while basic olfactory processing and the basal rate of adult-born neuron survival remained unaffected. Taken together these data indicate that survival of adult-born neurons during learning depends on consolidation processes taking place in the olfactory bulb.

Conclusion/significance: We can thus propose a model in which consolidation processes in the olfactory bulb determine both survival of adult-born neurons and long-term olfactory memory. The finding that adult-born neuron survival during olfactory learning is governed by consolidation in the olfactory bulb strongly argues in favor of a role for bulbar adult-born neurons in supporting olfactory memory.

Show MeSH
Related in: MedlinePlus