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Early calcium increase triggers the formation of olfactory long-term memory in honeybees.

Perisse E, Raymond-Delpech V, Néant I, Matsumoto Y, Leclerc C, Moreau M, Sandoz JC - BMC Biol. (2009)

Bottom Line: Synaptic plasticity associated with an important wave of gene transcription and protein synthesis underlies long-term memory processes.Calcium (Ca2+) plays an important role in a variety of neuronal functions and indirect evidence suggests that it may be involved in synaptic plasticity and in the regulation of gene expression correlated to long-term memory formation.Ca2+ therefore appears to act as a switch between short- and long-term storage of learned information.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centre de Recherches sur Cognition Animale, Université de Toulouse, CNRS, Toulouse, France. eperisse@cict.fr

ABSTRACT

Background: Synaptic plasticity associated with an important wave of gene transcription and protein synthesis underlies long-term memory processes. Calcium (Ca2+) plays an important role in a variety of neuronal functions and indirect evidence suggests that it may be involved in synaptic plasticity and in the regulation of gene expression correlated to long-term memory formation. The aim of this study was to determine whether Ca2+ is necessary and sufficient for inducing long-term memory formation. A suitable model to address this question is the Pavlovian appetitive conditioning of the proboscis extension reflex in the honeybee Apis mellifera, in which animals learn to associate an odor with a sucrose reward.

Results: By modulating the intracellular Ca2+ concentration ([Ca2+]i) in the brain, we show that: (i) blocking [Ca2+]i increase during multiple-trial conditioning selectively impairs long-term memory performance; (ii) conversely, increasing [Ca2+]i during single-trial conditioning triggers long-term memory formation; and finally, (iii) as was the case for long-term memory produced by multiple-trial conditioning, enhancement of long-term memory performance induced by a [Ca2+]i increase depends on de novo protein synthesis.

Conclusion: Altogether our data suggest that during olfactory conditioning Ca2+ is both a necessary and a sufficient signal for the formation of protein-dependent long-term memory. Ca2+ therefore appears to act as a switch between short- and long-term storage of learned information.

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Increase of [Ca2+]i using caffeine triggers long-term memory formation. Retention performances following an injection of caffeine (20 mM) or saline solution 20 min before one- or three-trial conditioning. A. Conditioned response (CR) to the learned odor at 72 h was significantly higher for the caffeine group (n = 60) than for the one-trial conditioning group (n = 78) (χ2 = 10.3, P = 0.0013), but not different from the three-trial conditioning group (n = 68) (χ2 = 1.64, P = 0.2). However, the response to the new odor was significantly different between the caffeine group and the one-trial conditioning (χ2 = 4.7, P = 0.03). Nevertheless, the caffeine group responded in the same way to the new odor than the three-trial conditioning group (χ2 = 3.2, P = 0.07). In addition, the control one-trial conditioning, the caffeine group and the control three-trial conditioning responded significantly more to the learned odor than to the new odor (respectively: McNemar χ2 = 14.4, P < 0.001; McNemar χ2 = 19.3, P < 0.001; McNemar χ2 = 23.3, P < 0.001). Overall, specific response (SR) proportion of the caffeine group was significantly increased compared with those of the control one-trial conditioning (χ2 = 3.9, P = 0.049) and was not different from the control three-trial conditioning (χ2 = 0.9, P = 0.33). B. The percentage of specific responses (% SR) for caffeine and for the control one-trial conditioning at 3 h (Control: n = 95; Caffeine: n = 78) and at 24 h (Control: n = 77; Caffeine: n = 84) were not affected by caffeine treatment (respectively: χ2 = 0.2, P = 0.62; χ2 = 0.8, P = 0.37). The % SR presented at 72 h corresponds to the data of Figure 3A (*: P < 0.05, **: P < 0.01, ***: P < 0.001, NS: non-significant).
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Figure 3: Increase of [Ca2+]i using caffeine triggers long-term memory formation. Retention performances following an injection of caffeine (20 mM) or saline solution 20 min before one- or three-trial conditioning. A. Conditioned response (CR) to the learned odor at 72 h was significantly higher for the caffeine group (n = 60) than for the one-trial conditioning group (n = 78) (χ2 = 10.3, P = 0.0013), but not different from the three-trial conditioning group (n = 68) (χ2 = 1.64, P = 0.2). However, the response to the new odor was significantly different between the caffeine group and the one-trial conditioning (χ2 = 4.7, P = 0.03). Nevertheless, the caffeine group responded in the same way to the new odor than the three-trial conditioning group (χ2 = 3.2, P = 0.07). In addition, the control one-trial conditioning, the caffeine group and the control three-trial conditioning responded significantly more to the learned odor than to the new odor (respectively: McNemar χ2 = 14.4, P < 0.001; McNemar χ2 = 19.3, P < 0.001; McNemar χ2 = 23.3, P < 0.001). Overall, specific response (SR) proportion of the caffeine group was significantly increased compared with those of the control one-trial conditioning (χ2 = 3.9, P = 0.049) and was not different from the control three-trial conditioning (χ2 = 0.9, P = 0.33). B. The percentage of specific responses (% SR) for caffeine and for the control one-trial conditioning at 3 h (Control: n = 95; Caffeine: n = 78) and at 24 h (Control: n = 77; Caffeine: n = 84) were not affected by caffeine treatment (respectively: χ2 = 0.2, P = 0.62; χ2 = 0.8, P = 0.37). The % SR presented at 72 h corresponds to the data of Figure 3A (*: P < 0.05, **: P < 0.01, ***: P < 0.001, NS: non-significant).

Mentions: For behavioral experiments, caffeine was injected 20 min prior to one-trial conditioning. The caffeine-elicited Ca2+ release during one-trial conditioning induced a strong increase in responses to the CS at 72 h, relative to saline injection (Figure 3A). This increased response reached a similar level to that obtained after three-trial conditioning. All groups responded significantly more to the learned odor than to the new odor. However, a significant response increase was also observed to the new odor in the caffeine group compared with the one-trial conditioning group. Such an increase is not surprising as there is some behavioral generalization from the learned odor to the new odor, and increasing memory for the learned odor through caffeine treatment may increase generalization responses to the novel odor [34]. As shown in Figure 3B at 72 h, caffeine treatment increased olfactory memory as the percentage of SR (% SR) was significantly increased relative to one-trial conditioning control. Caffeine treatment had to be associated with a conditioning trial, as caffeine injected 20 min before a CS-only presentation did not lead to any LTM performance (Additional file 2).


Early calcium increase triggers the formation of olfactory long-term memory in honeybees.

Perisse E, Raymond-Delpech V, Néant I, Matsumoto Y, Leclerc C, Moreau M, Sandoz JC - BMC Biol. (2009)

Increase of [Ca2+]i using caffeine triggers long-term memory formation. Retention performances following an injection of caffeine (20 mM) or saline solution 20 min before one- or three-trial conditioning. A. Conditioned response (CR) to the learned odor at 72 h was significantly higher for the caffeine group (n = 60) than for the one-trial conditioning group (n = 78) (χ2 = 10.3, P = 0.0013), but not different from the three-trial conditioning group (n = 68) (χ2 = 1.64, P = 0.2). However, the response to the new odor was significantly different between the caffeine group and the one-trial conditioning (χ2 = 4.7, P = 0.03). Nevertheless, the caffeine group responded in the same way to the new odor than the three-trial conditioning group (χ2 = 3.2, P = 0.07). In addition, the control one-trial conditioning, the caffeine group and the control three-trial conditioning responded significantly more to the learned odor than to the new odor (respectively: McNemar χ2 = 14.4, P < 0.001; McNemar χ2 = 19.3, P < 0.001; McNemar χ2 = 23.3, P < 0.001). Overall, specific response (SR) proportion of the caffeine group was significantly increased compared with those of the control one-trial conditioning (χ2 = 3.9, P = 0.049) and was not different from the control three-trial conditioning (χ2 = 0.9, P = 0.33). B. The percentage of specific responses (% SR) for caffeine and for the control one-trial conditioning at 3 h (Control: n = 95; Caffeine: n = 78) and at 24 h (Control: n = 77; Caffeine: n = 84) were not affected by caffeine treatment (respectively: χ2 = 0.2, P = 0.62; χ2 = 0.8, P = 0.37). The % SR presented at 72 h corresponds to the data of Figure 3A (*: P < 0.05, **: P < 0.01, ***: P < 0.001, NS: non-significant).
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Show All Figures
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Figure 3: Increase of [Ca2+]i using caffeine triggers long-term memory formation. Retention performances following an injection of caffeine (20 mM) or saline solution 20 min before one- or three-trial conditioning. A. Conditioned response (CR) to the learned odor at 72 h was significantly higher for the caffeine group (n = 60) than for the one-trial conditioning group (n = 78) (χ2 = 10.3, P = 0.0013), but not different from the three-trial conditioning group (n = 68) (χ2 = 1.64, P = 0.2). However, the response to the new odor was significantly different between the caffeine group and the one-trial conditioning (χ2 = 4.7, P = 0.03). Nevertheless, the caffeine group responded in the same way to the new odor than the three-trial conditioning group (χ2 = 3.2, P = 0.07). In addition, the control one-trial conditioning, the caffeine group and the control three-trial conditioning responded significantly more to the learned odor than to the new odor (respectively: McNemar χ2 = 14.4, P < 0.001; McNemar χ2 = 19.3, P < 0.001; McNemar χ2 = 23.3, P < 0.001). Overall, specific response (SR) proportion of the caffeine group was significantly increased compared with those of the control one-trial conditioning (χ2 = 3.9, P = 0.049) and was not different from the control three-trial conditioning (χ2 = 0.9, P = 0.33). B. The percentage of specific responses (% SR) for caffeine and for the control one-trial conditioning at 3 h (Control: n = 95; Caffeine: n = 78) and at 24 h (Control: n = 77; Caffeine: n = 84) were not affected by caffeine treatment (respectively: χ2 = 0.2, P = 0.62; χ2 = 0.8, P = 0.37). The % SR presented at 72 h corresponds to the data of Figure 3A (*: P < 0.05, **: P < 0.01, ***: P < 0.001, NS: non-significant).
Mentions: For behavioral experiments, caffeine was injected 20 min prior to one-trial conditioning. The caffeine-elicited Ca2+ release during one-trial conditioning induced a strong increase in responses to the CS at 72 h, relative to saline injection (Figure 3A). This increased response reached a similar level to that obtained after three-trial conditioning. All groups responded significantly more to the learned odor than to the new odor. However, a significant response increase was also observed to the new odor in the caffeine group compared with the one-trial conditioning group. Such an increase is not surprising as there is some behavioral generalization from the learned odor to the new odor, and increasing memory for the learned odor through caffeine treatment may increase generalization responses to the novel odor [34]. As shown in Figure 3B at 72 h, caffeine treatment increased olfactory memory as the percentage of SR (% SR) was significantly increased relative to one-trial conditioning control. Caffeine treatment had to be associated with a conditioning trial, as caffeine injected 20 min before a CS-only presentation did not lead to any LTM performance (Additional file 2).

Bottom Line: Synaptic plasticity associated with an important wave of gene transcription and protein synthesis underlies long-term memory processes.Calcium (Ca2+) plays an important role in a variety of neuronal functions and indirect evidence suggests that it may be involved in synaptic plasticity and in the regulation of gene expression correlated to long-term memory formation.Ca2+ therefore appears to act as a switch between short- and long-term storage of learned information.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centre de Recherches sur Cognition Animale, Université de Toulouse, CNRS, Toulouse, France. eperisse@cict.fr

ABSTRACT

Background: Synaptic plasticity associated with an important wave of gene transcription and protein synthesis underlies long-term memory processes. Calcium (Ca2+) plays an important role in a variety of neuronal functions and indirect evidence suggests that it may be involved in synaptic plasticity and in the regulation of gene expression correlated to long-term memory formation. The aim of this study was to determine whether Ca2+ is necessary and sufficient for inducing long-term memory formation. A suitable model to address this question is the Pavlovian appetitive conditioning of the proboscis extension reflex in the honeybee Apis mellifera, in which animals learn to associate an odor with a sucrose reward.

Results: By modulating the intracellular Ca2+ concentration ([Ca2+]i) in the brain, we show that: (i) blocking [Ca2+]i increase during multiple-trial conditioning selectively impairs long-term memory performance; (ii) conversely, increasing [Ca2+]i during single-trial conditioning triggers long-term memory formation; and finally, (iii) as was the case for long-term memory produced by multiple-trial conditioning, enhancement of long-term memory performance induced by a [Ca2+]i increase depends on de novo protein synthesis.

Conclusion: Altogether our data suggest that during olfactory conditioning Ca2+ is both a necessary and a sufficient signal for the formation of protein-dependent long-term memory. Ca2+ therefore appears to act as a switch between short- and long-term storage of learned information.

Show MeSH
Related in: MedlinePlus