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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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Anisomycin infusion in the olfactory bulb during the spaced learning blocked improvements in performance and increase in neurogenesis.A. Experimental design. BrdU was injected 14 days before training. Animals underwent spaced olfactory associative learning and were infused after each training session with either anisomycin or saline. Naive untrained animals were similarly infused with anisomycin or saline. A retention test was performed 5 days post-training. B. Behavioral performance. Conditioned saline-infused (saline C) animals learned the task as shown by the decrease in latency and remembered it after 5 days. In contrast, conditioned anisomycin-infused (aniso C) animals did not show any change in latency. C. Trial by trial analysis of the learning curve further showed that anisomycin-infused animals returned to pre-training performance between each training session in contrast to saline-infused animals. However, they showed within-session learning. Black arrows symbolize post-training bulbar infusions. D. Adult-born cell counts. Conditioning increased BrdU-positive cell density in saline-infused animals. The infusion of anisomycin prevented this effect without affecting the basal rate of neurogenesis. *: p<0.05; **: p<0.01; ns: non-significant (p>0.05).
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pone-0012118-g003: Anisomycin infusion in the olfactory bulb during the spaced learning blocked improvements in performance and increase in neurogenesis.A. Experimental design. BrdU was injected 14 days before training. Animals underwent spaced olfactory associative learning and were infused after each training session with either anisomycin or saline. Naive untrained animals were similarly infused with anisomycin or saline. A retention test was performed 5 days post-training. B. Behavioral performance. Conditioned saline-infused (saline C) animals learned the task as shown by the decrease in latency and remembered it after 5 days. In contrast, conditioned anisomycin-infused (aniso C) animals did not show any change in latency. C. Trial by trial analysis of the learning curve further showed that anisomycin-infused animals returned to pre-training performance between each training session in contrast to saline-infused animals. However, they showed within-session learning. Black arrows symbolize post-training bulbar infusions. D. Adult-born cell counts. Conditioning increased BrdU-positive cell density in saline-infused animals. The infusion of anisomycin prevented this effect without affecting the basal rate of neurogenesis. *: p<0.05; **: p<0.01; ns: non-significant (p>0.05).

Mentions: Animals were trained using the spaced paradigm, as for the first experiment. Immediately after the first training session, the mice were divided into two groups; one was infused in the OB with anisomycin (2 µL per OB, 100 µg/µL) and the other with saline. Intra-bulbar infusions were performed 10 min after the end of each training session (Figure 3A). Performances in the anisomycin- and saline-treated groups were different (group effect, F(1,17) = 4.592, p<0.05). We found that the behavioral task was rapidly acquired in the saline-injected animals as evidenced by the decrease in latency with time (day effect, F(4,45) = 12.842, p<0.001) (Figure 3B) and the increase in their success rate (day effect, F(4,45) = 11.69, p<0.001). However in the anisomycin-infused animals, no change in latency (day effect, F(4,40) = 0.532, p>0.05) (Figure 3B) or in success rate (day effect, F(4,40) = 2.38, p>0.05) was observed indicating that the protein synthesis blocker altered learning of the associative olfactory task.


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)

Anisomycin infusion in the olfactory bulb during the spaced learning blocked improvements in performance and increase in neurogenesis.A. Experimental design. BrdU was injected 14 days before training. Animals underwent spaced olfactory associative learning and were infused after each training session with either anisomycin or saline. Naive untrained animals were similarly infused with anisomycin or saline. A retention test was performed 5 days post-training. B. Behavioral performance. Conditioned saline-infused (saline C) animals learned the task as shown by the decrease in latency and remembered it after 5 days. In contrast, conditioned anisomycin-infused (aniso C) animals did not show any change in latency. C. Trial by trial analysis of the learning curve further showed that anisomycin-infused animals returned to pre-training performance between each training session in contrast to saline-infused animals. However, they showed within-session learning. Black arrows symbolize post-training bulbar infusions. D. Adult-born cell counts. Conditioning increased BrdU-positive cell density in saline-infused animals. The infusion of anisomycin prevented this effect without affecting the basal rate of neurogenesis. *: p<0.05; **: p<0.01; ns: non-significant (p>0.05).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2921340&req=5

pone-0012118-g003: Anisomycin infusion in the olfactory bulb during the spaced learning blocked improvements in performance and increase in neurogenesis.A. Experimental design. BrdU was injected 14 days before training. Animals underwent spaced olfactory associative learning and were infused after each training session with either anisomycin or saline. Naive untrained animals were similarly infused with anisomycin or saline. A retention test was performed 5 days post-training. B. Behavioral performance. Conditioned saline-infused (saline C) animals learned the task as shown by the decrease in latency and remembered it after 5 days. In contrast, conditioned anisomycin-infused (aniso C) animals did not show any change in latency. C. Trial by trial analysis of the learning curve further showed that anisomycin-infused animals returned to pre-training performance between each training session in contrast to saline-infused animals. However, they showed within-session learning. Black arrows symbolize post-training bulbar infusions. D. Adult-born cell counts. Conditioning increased BrdU-positive cell density in saline-infused animals. The infusion of anisomycin prevented this effect without affecting the basal rate of neurogenesis. *: p<0.05; **: p<0.01; ns: non-significant (p>0.05).
Mentions: Animals were trained using the spaced paradigm, as for the first experiment. Immediately after the first training session, the mice were divided into two groups; one was infused in the OB with anisomycin (2 µL per OB, 100 µg/µL) and the other with saline. Intra-bulbar infusions were performed 10 min after the end of each training session (Figure 3A). Performances in the anisomycin- and saline-treated groups were different (group effect, F(1,17) = 4.592, p<0.05). We found that the behavioral task was rapidly acquired in the saline-injected animals as evidenced by the decrease in latency with time (day effect, F(4,45) = 12.842, p<0.001) (Figure 3B) and the increase in their success rate (day effect, F(4,45) = 11.69, p<0.001). However in the anisomycin-infused animals, no change in latency (day effect, F(4,40) = 0.532, p>0.05) (Figure 3B) or in success rate (day effect, F(4,40) = 2.38, p>0.05) was observed indicating that the protein synthesis blocker altered learning of the associative olfactory task.

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