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

Perisse E, Raymond-Delpech V, Nテゥant 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, Universitテゥ 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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Caffeine induces a transient Ca2+increase in the honeybee brain. Relative fluorescence changes (% ホ認/F0) in the antennal lobe (AL) after an application of 10 ホシl of 20 mM caffeine (n = 10) or saline (n = 7) 10 min after the start of the recording (black arrow) and during 50 minutes. Between 10 and 24 min after caffeine application, the % ホ認/F0 recorded for the caffeine animals is significantly higher than for the control animals. (*: P < 0.05, t-test). Note that the drop in fluorescence observed in the saline recording is due to a change in the volume of solution between brain and objective.
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Figure 2: Caffeine induces a transient Ca2+increase in the honeybee brain. Relative fluorescence changes (% ホ認/F0) in the antennal lobe (AL) after an application of 10 ホシl of 20 mM caffeine (n = 10) or saline (n = 7) 10 min after the start of the recording (black arrow) and during 50 minutes. Between 10 and 24 min after caffeine application, the % ホ認/F0 recorded for the caffeine animals is significantly higher than for the control animals. (*: P < 0.05, t-test). Note that the drop in fluorescence observed in the saline recording is due to a change in the volume of solution between brain and objective.

Mentions: The previous experiment shows that Ca2+ is necessary to establish LTM, but is it sufficient? To answer this question we increased [Ca2+]i during one-trial conditioning, a training protocol normally inefficient to produce LTM [27]. Caffeine, which induces the release of Ca2+ from ryanodine-sensitive stores [33], was used to increase [Ca2+]i in the honeybee brain. As a prerequisite for this experiment, we confirmed with Ca2+ imaging experiments that an injection of caffeine (20 mM) induces an increase of [Ca2+]i. The Ca2+ signal was recorded during 60 min in three different olfactory structures (antennal lobe, alpha lobe of the mushroom bodies and lateral protocerebrum). After 10 min of recording, caffeine solution or saline was injected. As shown for the antennal lobe (Figure 2), and also for the two other recorded structures, caffeine application significantly increased [Ca2+]i during a 14-min time window, compared with saline application.


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

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

Caffeine induces a transient Ca2+increase in the honeybee brain. Relative fluorescence changes (% ホ認/F0) in the antennal lobe (AL) after an application of 10 ホシl of 20 mM caffeine (n = 10) or saline (n = 7) 10 min after the start of the recording (black arrow) and during 50 minutes. Between 10 and 24 min after caffeine application, the % ホ認/F0 recorded for the caffeine animals is significantly higher than for the control animals. (*: P < 0.05, t-test). Note that the drop in fluorescence observed in the saline recording is due to a change in the volume of solution between brain and objective.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Caffeine induces a transient Ca2+increase in the honeybee brain. Relative fluorescence changes (% ホ認/F0) in the antennal lobe (AL) after an application of 10 ホシl of 20 mM caffeine (n = 10) or saline (n = 7) 10 min after the start of the recording (black arrow) and during 50 minutes. Between 10 and 24 min after caffeine application, the % ホ認/F0 recorded for the caffeine animals is significantly higher than for the control animals. (*: P < 0.05, t-test). Note that the drop in fluorescence observed in the saline recording is due to a change in the volume of solution between brain and objective.
Mentions: The previous experiment shows that Ca2+ is necessary to establish LTM, but is it sufficient? To answer this question we increased [Ca2+]i during one-trial conditioning, a training protocol normally inefficient to produce LTM [27]. Caffeine, which induces the release of Ca2+ from ryanodine-sensitive stores [33], was used to increase [Ca2+]i in the honeybee brain. As a prerequisite for this experiment, we confirmed with Ca2+ imaging experiments that an injection of caffeine (20 mM) induces an increase of [Ca2+]i. The Ca2+ signal was recorded during 60 min in three different olfactory structures (antennal lobe, alpha lobe of the mushroom bodies and lateral protocerebrum). After 10 min of recording, caffeine solution or saline was injected. As shown for the antennal lobe (Figure 2), and also for the two other recorded structures, caffeine application significantly increased [Ca2+]i during a 14-min time window, compared with saline application.

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, Universitテゥ 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