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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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Inhibition of [Ca2+]i increase using BAPTA-AM blocks long-term memory formation. Acquisition and retention performances following an injection of BAPTA-AM 500 μM, an intracellular Ca2+ chelator, or saline 1 h before training. A. Percentages of conditioned responses (%CR) increase during the three conditioning trials (C1, C2 and C3) for the control group (n = 70, Q = 60.0, P < 0.001) and for the BAPTA-AM group (n = 85, Q = 81.0, P < 0.001), without any difference between groups (U = 278.5, P = 0.93). Response to the conditioned stimulus (CS) after 72 h was significantly lower in the BAPTA-AM than in the control group (χ2 = 9.1, P = 0.0026). Moreover, bees responded significantly more to the CS than to the new odor in the control group (χ2 = 24.3, P < 0.001) but not in the BAPTA-AM group (χ2 = 2.0, P = 0.15). Consequently, specific response proportion (% individuals responding to the CS and not to the new odor) was significantly lower for BAPTA-AM than for control bees (χ2 = 15.55, P < 0.001). Furthermore, control and treated animals responded similarly to the new odor (χ2 = 2.25, P = 0.13). B. The percentage of specific response (% SR) at 3 h (Control: n = 125; BAPTA-AM: n = 120) and 24 h (Control: n = 112; BAPTA-AM: n = 117) were not affected by treatment with BAPTA-AM (respectively: χ2 = 0.65, P = 0.42 and χ2 = 0.43, P = 0.51). The % SR presented at 72 h corresponds to the data of Figure 1A. (***: P < 0.001, NS: non-significant).
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Figure 1: Inhibition of [Ca2+]i increase using BAPTA-AM blocks long-term memory formation. Acquisition and retention performances following an injection of BAPTA-AM 500 μM, an intracellular Ca2+ chelator, or saline 1 h before training. A. Percentages of conditioned responses (%CR) increase during the three conditioning trials (C1, C2 and C3) for the control group (n = 70, Q = 60.0, P < 0.001) and for the BAPTA-AM group (n = 85, Q = 81.0, P < 0.001), without any difference between groups (U = 278.5, P = 0.93). Response to the conditioned stimulus (CS) after 72 h was significantly lower in the BAPTA-AM than in the control group (χ2 = 9.1, P = 0.0026). Moreover, bees responded significantly more to the CS than to the new odor in the control group (χ2 = 24.3, P < 0.001) but not in the BAPTA-AM group (χ2 = 2.0, P = 0.15). Consequently, specific response proportion (% individuals responding to the CS and not to the new odor) was significantly lower for BAPTA-AM than for control bees (χ2 = 15.55, P < 0.001). Furthermore, control and treated animals responded similarly to the new odor (χ2 = 2.25, P = 0.13). B. The percentage of specific response (% SR) at 3 h (Control: n = 125; BAPTA-AM: n = 120) and 24 h (Control: n = 112; BAPTA-AM: n = 117) were not affected by treatment with BAPTA-AM (respectively: χ2 = 0.65, P = 0.42 and χ2 = 0.43, P = 0.51). The % SR presented at 72 h corresponds to the data of Figure 1A. (***: P < 0.001, NS: non-significant).

Mentions: Three conditioning trials with 10-min inter-trial intervals normally lead to high LTM performance at 72 h. To test whether Ca2+ is necessary for LTM formation, we first evaluated the effect of 1,2-bis-(o-aminophenoxy)-ethane-N,N,N',N'-tetraacetic acid, tetraacetoxymethyl ester (BAPTA-AM), a membrane permeant Ca2+ chelator, injected 1 h before conditioning on memory performance at 72 h. The results in Figure 1A (left panel) show that the percentage of conditioned responses (%CR) increased similarly during conditioning in BAPTA-treated and control animals, indicating that BAPTA treatment does not affect acquisition performance. However, as shown on the histogram of Figure 1A (right panel, black bars), after 72 h the responses to the learned odor (CS) were significantly reduced in BAPTA-treated animals, relative to controls. To check whether memory was specific to the learned odor, we systematically compared performance to the CS and to a new odor in the two groups (Figure 1A, grey bars right panel). After 72 h, while control animals responded significantly less to a new odor than to the CS, BAPTA-treated animals responded similarly to both stimuli. Furthermore, control and BAPTA-treated animals responded similarly to the new odor. All these data indicate that control animals have strong CS-specific LTM while BAPTA-treated animals present no such specific LTM.


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)

Inhibition of [Ca2+]i increase using BAPTA-AM blocks long-term memory formation. Acquisition and retention performances following an injection of BAPTA-AM 500 μM, an intracellular Ca2+ chelator, or saline 1 h before training. A. Percentages of conditioned responses (%CR) increase during the three conditioning trials (C1, C2 and C3) for the control group (n = 70, Q = 60.0, P < 0.001) and for the BAPTA-AM group (n = 85, Q = 81.0, P < 0.001), without any difference between groups (U = 278.5, P = 0.93). Response to the conditioned stimulus (CS) after 72 h was significantly lower in the BAPTA-AM than in the control group (χ2 = 9.1, P = 0.0026). Moreover, bees responded significantly more to the CS than to the new odor in the control group (χ2 = 24.3, P < 0.001) but not in the BAPTA-AM group (χ2 = 2.0, P = 0.15). Consequently, specific response proportion (% individuals responding to the CS and not to the new odor) was significantly lower for BAPTA-AM than for control bees (χ2 = 15.55, P < 0.001). Furthermore, control and treated animals responded similarly to the new odor (χ2 = 2.25, P = 0.13). B. The percentage of specific response (% SR) at 3 h (Control: n = 125; BAPTA-AM: n = 120) and 24 h (Control: n = 112; BAPTA-AM: n = 117) were not affected by treatment with BAPTA-AM (respectively: χ2 = 0.65, P = 0.42 and χ2 = 0.43, P = 0.51). The % SR presented at 72 h corresponds to the data of Figure 1A. (***: P < 0.001, NS: non-significant).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC2713209&req=5

Figure 1: Inhibition of [Ca2+]i increase using BAPTA-AM blocks long-term memory formation. Acquisition and retention performances following an injection of BAPTA-AM 500 μM, an intracellular Ca2+ chelator, or saline 1 h before training. A. Percentages of conditioned responses (%CR) increase during the three conditioning trials (C1, C2 and C3) for the control group (n = 70, Q = 60.0, P < 0.001) and for the BAPTA-AM group (n = 85, Q = 81.0, P < 0.001), without any difference between groups (U = 278.5, P = 0.93). Response to the conditioned stimulus (CS) after 72 h was significantly lower in the BAPTA-AM than in the control group (χ2 = 9.1, P = 0.0026). Moreover, bees responded significantly more to the CS than to the new odor in the control group (χ2 = 24.3, P < 0.001) but not in the BAPTA-AM group (χ2 = 2.0, P = 0.15). Consequently, specific response proportion (% individuals responding to the CS and not to the new odor) was significantly lower for BAPTA-AM than for control bees (χ2 = 15.55, P < 0.001). Furthermore, control and treated animals responded similarly to the new odor (χ2 = 2.25, P = 0.13). B. The percentage of specific response (% SR) at 3 h (Control: n = 125; BAPTA-AM: n = 120) and 24 h (Control: n = 112; BAPTA-AM: n = 117) were not affected by treatment with BAPTA-AM (respectively: χ2 = 0.65, P = 0.42 and χ2 = 0.43, P = 0.51). The % SR presented at 72 h corresponds to the data of Figure 1A. (***: P < 0.001, NS: non-significant).
Mentions: Three conditioning trials with 10-min inter-trial intervals normally lead to high LTM performance at 72 h. To test whether Ca2+ is necessary for LTM formation, we first evaluated the effect of 1,2-bis-(o-aminophenoxy)-ethane-N,N,N',N'-tetraacetic acid, tetraacetoxymethyl ester (BAPTA-AM), a membrane permeant Ca2+ chelator, injected 1 h before conditioning on memory performance at 72 h. The results in Figure 1A (left panel) show that the percentage of conditioned responses (%CR) increased similarly during conditioning in BAPTA-treated and control animals, indicating that BAPTA treatment does not affect acquisition performance. However, as shown on the histogram of Figure 1A (right panel, black bars), after 72 h the responses to the learned odor (CS) were significantly reduced in BAPTA-treated animals, relative to controls. To check whether memory was specific to the learned odor, we systematically compared performance to the CS and to a new odor in the two groups (Figure 1A, grey bars right panel). After 72 h, while control animals responded significantly less to a new odor than to the CS, BAPTA-treated animals responded similarly to both stimuli. Furthermore, control and BAPTA-treated animals responded similarly to the new odor. All these data indicate that control animals have strong CS-specific LTM while BAPTA-treated animals present no such specific LTM.

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