Delayed Intrinsic Activation of an NMDA-Independent CaM-kinase II in a Critical Time Window Is Necessary for Late Consolidation of an Associative Memory

Wan, Huihui; Mackay, Beth; Iqbal, Hassan; Naskar, Souvik; Kemenes, György

doi:10.1523/jneurosci.2577-09.2010

Cited by 26 publications

(25 citation statements)

References 46 publications

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“…Among these kinases, only ErK1/2 is activated in both processes (Atkins et al, 1998;Fischer et al, 2007;Irvine et al, 2005;Kimura et al, 2008;Tronson et al, 2012). Moreover, Erk1/2 is critical for the late consolidation of fear memory (Bekinschtein et al, 2007;Wan et al, 2010). In the present study, we found that Erk1/2 was activated in the late phase after extinction and was unaffected by NE.…”

Section: Mechanism That Underlies the Role Of Hippocampal Ne In The Psupporting

confidence: 55%

Delayed Noradrenergic Activation in the Dorsal Hippocampus Promotes the Long-Term Persistence of Extinguished Fear

Chai

Liu

Xue

et al. 2014

Neuropsychopharmacol

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Fear extinction has been extensively studied, but little is known about the molecular processes that underlie the persistence of extinction long-term memory (LTM). We found that microinfusion of norepinephrine (NE) into the CA1 area of the dorsal hippocampus during the early phase (0 h) after extinction enhanced extinction LTM at 2 and 14 days after extinction. Intra-CA1 infusion of NE during the late phase (12 h) after extinction selectively promoted extinction LTM at 14 days after extinction that was blocked by the b-receptor antagonist propranolol, protein kinase A (PKA) inhibitor Rp-cAMPS, and protein synthesis inhibitors anisomycin and emetine. The phosphorylation levels of PKA, cyclic adenosine monophosphate response element-binding protein (CREB), GluR1, and the membrane GluR1 level were increased by NE during the late phase after extinction that was also blocked by propranolol and Rp-cAMPS. These results suggest that the enhancement of extinction LTM persistence induced by NE requires the activation of the b-receptor/PKA/CREB signaling pathway and membrane GluR1 trafficking. Moreover, extinction increased the phosphorylation levels of Erk1/2, CREB, and GluR1, and the membrane GluR1 level during the late phase, and anisomycin/emetine alone disrupted the persistence of extinction LTM, indicating that the persistence of extinction LTM requires late-phase protein synthesis in the CA1. Propranolol and Rp-cAMPS did not completely disrupt the persistence of extinction LTM, suggesting that another b-receptor/PKA-independent mechanism underlies the persistence of extinction LTM. Altogether, our results showed that enhancing hippocampal noradrenergic activity during the late phase after extinction selectively promotes the persistence of extinction LTM.

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Section: Mechanism That Underlies the Role Of Hippocampal Ne In The Psupporting

confidence: 55%

Delayed Noradrenergic Activation in the Dorsal Hippocampus Promotes the Long-Term Persistence of Extinguished Fear

Chai

Liu

Xue

et al. 2014

Neuropsychopharmacol

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“…A model of the PACAP-activated molecular cascades of memory formation after food-reward classical conditioning in Lymnaea Previous molecular, behavioral, pharmacological, and electrophysiological analyses already have identified a number of receptors, ion channels, and signaling molecules involved in the acquisition as well as early and/or late consolidation of associative LTM after food-reward classical conditioning in Lymnaea Ribeiro et al, 2003Ribeiro et al, , 2005Ribeiro et al, , 2008Fulton et al, 2005;Korneev et al, 2005;Michel et al, 2008;Nikitin et al, 2008;Wan et al, 2010). Our new findings have now made it possible to construct a model of the interacting components involved in the formation of long-term associative memory after foodreward classical conditioning in Lymnaea (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…6). The activation of these molecules is necessary for early consolidation of long-term memory Ribeiro et al, 2005;Michel et al, 2008;Wan et al, 2010), and all of them can be linked, either directly or indirectly, to the initial activation of AC (Fig. 6).…”

Section: Discussionmentioning

confidence: 99%

A Homolog of the Vertebrate Pituitary Adenylate Cyclase-Activating Polypeptide Is Both Necessary and Instructive for the Rapid Formation of Associative Memory in an Invertebrate

Pirger

László²,

Kemenes³

et al. 2010

J. Neurosci.

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Similar to other invertebrate and vertebrate animals, cAMP-dependent signaling cascades are key components of long-term memory (LTM) formation in the snail Lymnaea stagnalis, an established experimental model for studying evolutionarily conserved molecular mechanisms of long-term associative memory. Although a great deal is already known about the signaling cascades activated by cAMP, the molecules involved in the learning-induced activation of adenylate cyclase (AC) in Lymnaea remained unknown.Using matrix-assisted laser desorption/ionization time-of-flight mass spectroscopy in combination with biochemical and immunohistochemical methods, recently we have obtained evidence for the existence of a Lymnaea homolog of the vertebrate pituitary adenylate cyclaseactivating polypeptide (PACAP) and for the AC-activating effect of PACAP in the Lymnaea nervous system. Here we first tested the hypothesis that PACAP plays an important role in the formation of robust LTM after single-trial classical food-reward conditioning. Application of the PACAP receptor antagonist PACAP6-38 around the time of single-trial training with amyl acetate and sucrose blocked associative LTM, suggesting that in this "strong" food-reward conditioning paradigm the activation of AC by PACAP was necessary for LTM to form. We found that in a "weak" multitrial food-reward conditioning paradigm, lip touch paired with sucrose, memory formation was also dependent on PACAP. Significantly, systemic application of PACAP at the beginning of multitrial tactile conditioning accelerated the formation of transcriptiondependent memory.Our findings provide the first evidence to show that in the same nervous system PACAP is both necessary and instructive for fast and robust memory formation after reward classical conditioning.

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“…In the pond snail Lymnaea stagnalis, for instance, CaMKII is necessary for acquisition and late consolidation, but not early or intermediate consolidation or retrieval of LTM (Wan et al 2010). In Drosophila, CaMKII is necessary for courtship-associated learning and memory (Mehren and Griffith 2004) and for LTM formation following odor-shock pairing (Akalal et al 2010).…”

Section: The Role Of Camkii In L-ltm Formation In Honeybeesmentioning

confidence: 99%

Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee

et al. 2014

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Memory is a dynamic process that allows encoding, storage, and retrieval of information acquired through individual experience. In the honeybee Apis mellifera, olfactory conditioning of the proboscis extension response (PER) has shown that besides short-term memory (STM) and mid-term memory (MTM), two phases of long-term memory (LTM) are formed upon multiple-trial conditioning: an early phase (e-LTM) which depends on translation from already available mRNA, and a late phase (l-LTM) which requires de novo transcription and translation. Here we combined olfactory PER conditioning and neuropharmacological inhibition and studied the involvement of the NO-cGMP pathway, and of specific molecules, such as cyclic nucleotide-gated channels (CNG), calmodulin (CaM), adenylyl cyclase (AC), and Ca 2+ /calmodulin-dependent protein kinase (CaMKII), in the formation of olfactory LTM in bees. We show that in addition to NO-cGMP and cAMP-PKA, CNG channels, CaM, AC, and CaMKII also participate in the formation of a l-LTM (72-h post-conditioning) that is specific for the learned odor. Importantly, the same molecules are dispensable for olfactory learning and for the formation of both MTM (in the minute and hour range) and e-LTM (24-h post-conditioning), thus suggesting that the signaling pathways leading to l-LTM or e-LTM involve different molecular actors.

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Delayed Intrinsic Activation of an NMDA-Independent CaM-kinase II in a Critical Time Window Is Necessary for Late Consolidation of an Associative Memory

Cited by 26 publications

References 46 publications

Delayed Noradrenergic Activation in the Dorsal Hippocampus Promotes the Long-Term Persistence of Extinguished Fear

Delayed Noradrenergic Activation in the Dorsal Hippocampus Promotes the Long-Term Persistence of Extinguished Fear

A Homolog of the Vertebrate Pituitary Adenylate Cyclase-Activating Polypeptide Is Both Necessary and Instructive for the Rapid Formation of Associative Memory in an Invertebrate

Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee

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