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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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Long-term memory increase induced by Ca2+ is dependent on de novo gene transcription. Control bees are compared with bees that received an injection of actinomycin-D (ACT-D) 3 h after conditioning. In control bees (black bars), injection of caffeine 20 min before one-trial conditioning induced a significant increase in retention performance (percentage of specific response, % SR, % individuals responding to the conditioned stimulus and not to the new odor) at 72 h, compared with bees which received a one-trial conditioning (χ2 = 10.41, P = 0.0013). This replicates the results shown in Figure 3. Bees which received three conditioning trials showed high long-term memory (LTM) performance, as usual. Injection of ACT-D (white bars) almost totally erased the promnesic effect of caffeine, so that there was no longer any difference between one-trial and one-trial plus caffeine bees. Bees of the caffeine group injected with ACT-D (n = 62) thus showed a significant decrease of SR compared with control bees (n = 61) (χ2 = 16.62, P < 0.001). No difference appears for the control one trial conditioning (χ2 = 0.24, P = 0.62; Control: n = 64; ACT-D: n = 69). LTM produced by three-trial conditioning was also utterly erased (χ2 = 40.29, P < 0.001; control: n = 63; ACT-D: n = 70).
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Figure 5: Long-term memory increase induced by Ca2+ is dependent on de novo gene transcription. Control bees are compared with bees that received an injection of actinomycin-D (ACT-D) 3 h after conditioning. In control bees (black bars), injection of caffeine 20 min before one-trial conditioning induced a significant increase in retention performance (percentage of specific response, % SR, % individuals responding to the conditioned stimulus and not to the new odor) at 72 h, compared with bees which received a one-trial conditioning (χ2 = 10.41, P = 0.0013). This replicates the results shown in Figure 3. Bees which received three conditioning trials showed high long-term memory (LTM) performance, as usual. Injection of ACT-D (white bars) almost totally erased the promnesic effect of caffeine, so that there was no longer any difference between one-trial and one-trial plus caffeine bees. Bees of the caffeine group injected with ACT-D (n = 62) thus showed a significant decrease of SR compared with control bees (n = 61) (χ2 = 16.62, P < 0.001). No difference appears for the control one trial conditioning (χ2 = 0.24, P = 0.62; Control: n = 64; ACT-D: n = 69). LTM produced by three-trial conditioning was also utterly erased (χ2 = 40.29, P < 0.001; control: n = 63; ACT-D: n = 70).

Mentions: LTM is dependent on a new wave of protein synthesis, required for the functional and structural synaptic modifications involved in long-term storage of information [6,30]. To test whether the LTM formed after an increase in [Ca2+]i is dependent upon protein synthesis, we replicated the previous experiment in the presence of the transcription inhibitor, actinomycin-D (ACT-D). Bees were subjected to one-trial conditioning associated with the injection of caffeine (20 mM) or saline solution, followed 3 h later either by an injection of ACT-D (experimental group) or saline solution (control group). These groups were then tested at 72 h. As shown in Figure 5, performance in the one-trial group injected with caffeine was significantly higher than in the one-trial control group, reproducing the previous induction of LTM by caffeine. This increase of SR performance was totally erased in the corresponding experimental group injected with ACT-D, so that performance was equivalent to that in the one-trial control group. We also performed a control experiment with three-trial conditioning which received or not ACT-D. Performances of this control three-trials conditioning group were strongly affected by ACT-D injection, as already described in the literature [38]. Thus, the increase in LTM performances in the caffeine-injected one-trial group is associated with de novo protein synthesis during consolidation.


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)

Long-term memory increase induced by Ca2+ is dependent on de novo gene transcription. Control bees are compared with bees that received an injection of actinomycin-D (ACT-D) 3 h after conditioning. In control bees (black bars), injection of caffeine 20 min before one-trial conditioning induced a significant increase in retention performance (percentage of specific response, % SR, % individuals responding to the conditioned stimulus and not to the new odor) at 72 h, compared with bees which received a one-trial conditioning (χ2 = 10.41, P = 0.0013). This replicates the results shown in Figure 3. Bees which received three conditioning trials showed high long-term memory (LTM) performance, as usual. Injection of ACT-D (white bars) almost totally erased the promnesic effect of caffeine, so that there was no longer any difference between one-trial and one-trial plus caffeine bees. Bees of the caffeine group injected with ACT-D (n = 62) thus showed a significant decrease of SR compared with control bees (n = 61) (χ2 = 16.62, P < 0.001). No difference appears for the control one trial conditioning (χ2 = 0.24, P = 0.62; Control: n = 64; ACT-D: n = 69). LTM produced by three-trial conditioning was also utterly erased (χ2 = 40.29, P < 0.001; control: n = 63; ACT-D: n = 70).
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Figure 5: Long-term memory increase induced by Ca2+ is dependent on de novo gene transcription. Control bees are compared with bees that received an injection of actinomycin-D (ACT-D) 3 h after conditioning. In control bees (black bars), injection of caffeine 20 min before one-trial conditioning induced a significant increase in retention performance (percentage of specific response, % SR, % individuals responding to the conditioned stimulus and not to the new odor) at 72 h, compared with bees which received a one-trial conditioning (χ2 = 10.41, P = 0.0013). This replicates the results shown in Figure 3. Bees which received three conditioning trials showed high long-term memory (LTM) performance, as usual. Injection of ACT-D (white bars) almost totally erased the promnesic effect of caffeine, so that there was no longer any difference between one-trial and one-trial plus caffeine bees. Bees of the caffeine group injected with ACT-D (n = 62) thus showed a significant decrease of SR compared with control bees (n = 61) (χ2 = 16.62, P < 0.001). No difference appears for the control one trial conditioning (χ2 = 0.24, P = 0.62; Control: n = 64; ACT-D: n = 69). LTM produced by three-trial conditioning was also utterly erased (χ2 = 40.29, P < 0.001; control: n = 63; ACT-D: n = 70).
Mentions: LTM is dependent on a new wave of protein synthesis, required for the functional and structural synaptic modifications involved in long-term storage of information [6,30]. To test whether the LTM formed after an increase in [Ca2+]i is dependent upon protein synthesis, we replicated the previous experiment in the presence of the transcription inhibitor, actinomycin-D (ACT-D). Bees were subjected to one-trial conditioning associated with the injection of caffeine (20 mM) or saline solution, followed 3 h later either by an injection of ACT-D (experimental group) or saline solution (control group). These groups were then tested at 72 h. As shown in Figure 5, performance in the one-trial group injected with caffeine was significantly higher than in the one-trial control group, reproducing the previous induction of LTM by caffeine. This increase of SR performance was totally erased in the corresponding experimental group injected with ACT-D, so that performance was equivalent to that in the one-trial control group. We also performed a control experiment with three-trial conditioning which received or not ACT-D. Performances of this control three-trials conditioning group were strongly affected by ACT-D injection, as already described in the literature [38]. Thus, the increase in LTM performances in the caffeine-injected one-trial group is associated with de novo protein synthesis during consolidation.

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