Requirement of New Protein Synthesis of a Transcription Factor for Memory Consolidation: Paradoxical Changes in mRNA and Protein Levels of C/EBP

Hatakeyama, Dai; Sadamoto, Hisayo; Watanabe, Takayuki; Wagatsuma, Akiko; Kobayashi, Suguru; Fujito, Yutaka; Yamashita, Masakane; Sakakibara, Manabu; Kemenes, György; Ito, Etsuro

doi:10.1016/j.jmb.2005.12.009

Cited by 52 publications

(49 citation statements)

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“…It has been hypothesized that the cerebral giant cells and the B2 motor neurons play key roles in mediating the learning and LTM formation of this CTA (Kojima et al, 1997;Kojima et al, 2000;Kojima et al, 2001;Hatakeyama et al, 2004a;Sadamoto et al, 2004b). Consistent with this hypothesis are the data showing that altered gene activity and new protein synthesis must occur in these and other neurons if LTM is to form following the CTA procedure Hatakeyama et al, 2004b;Hatakeyama et al, 2006;Azami et al, 2006;Wagatsuma et al, 2006). In addition, our recent findings showed that snails are both able to discriminate different tastes and continue to eat other foods following the CTA procedure (Sugai et al, 2006).…”

Section: Introductionmentioning

confidence: 76%

One-trial conditioned taste aversion inLymnaea: good and poor performers in long-term memory acquisition

Sugai

Azami

Shiga

et al. 2007

Journal of Experimental Biology

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In the majority of studies designed to elucidate the causal mechanisms of memory formation, certain members of the experimental cohort, even though subjected to exactly the same conditioning procedures, remember significantly better than others, whereas others show little or no long-term memory (LTM) formation. To begin to address the question of why this phenomenon occurs and thereby help clarify the causal mechanism of LTM formation, we used a conditioned taste aversion (CTA) procedure on individuals of the pond snail Lymnaea stagnalis and analyzed their subsequent behavior. Using sucrose as an appetitive stimulus and KCl as an aversive stimulus, we obtained a constant ratio of 'poor' to 'good' performers for CTA-LTM. We found that approximately 40% of trained snails possessed LTM following a one-trial conditioning procedure. When we examined the timewindow necessary for the memory consolidation, we found that if we cooled snails to 4°C for 30·min within 10·min after the one-trial conditioning, LTM was blocked. However, with delayed cooling (i.e. longer than 10·min), LTM was present. We could further interfere with LTM formation by inducing inhibitory learning (i.e. backward conditioning) after the one-trial conditioning. Finally, we examined whether we could motivate snails to acquire LTM by depriving them of food for 5·days before the onetrial conditioning. Food-deprived snails, however, failed to exhibit LTM following the one-trial conditioning. These results will help us begin to clarify why some individuals are better at learning and forming memory for specific tasks at the neuronal level.

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Section: Introductionmentioning

confidence: 76%

One-trial conditioned taste aversion inLymnaea: good and poor performers in long-term memory acquisition

Sugai

Azami

Shiga

et al. 2007

Journal of Experimental Biology

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“…However, we cannot rule out the possibility that ApC/EBP mRNA and protein are induced as specific results of the training procedure but are unrelated to long-term memory formation. This possibility seems unlikely, given the established role of ApC/ EBP in the formation of long-term plasticity in other systems (Alberini et al 1994;Taubenfeld et al 2001;Hatakeyama et al 2006;Yefet et al 2006).…”

Section: C/ebp Inmentioning

confidence: 99%

Training with inedible food in Aplysia causes expression of C/EBP in the buccal but not cerebral ganglion

Levitan

Lyons²,

Perelman³

et al. 2008

Learn. Mem.

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Training with inedible food in Aplysia increased expression of the transcription factor C/EBP in the buccal ganglia, which primarily have a motor function, but not in the cerebral or pleural ganglia. C/EBP mRNA increased immediately after training, as well as 1–2 h later. The increased expression of C/EBP protein lagged the increase in mRNA. Stimulating the lips and inducing feeding responses do not lead to long-term memory and did not cause increased C/EBP expression. Blocking polyADP-ribosylation, a process necessary for long-term memory after training, did not affect the increased C/EBP mRNA expression in the buccal ganglia.

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“…First, changes in the expression of ApC/EBP may not be restricted to the buccal ganglia mechanoafferents, as was shown in conditioned taste aversion in Lymnaea (Hatakeyama et al 2006). When examining tissues such as the non-mechanoafferent components of the buccal ganglia or the cerebral ganglion, even large changes in a small number of cells may not be detected.…”

Section: Discussionmentioning

confidence: 98%

“…These changes are then expressed as a change in behavior. A first step in understanding how molecular processes cause behavioral change is to localize the molecular processes to specific neuron populations (Gusev et al 2005;Hatakeyama et al 2006;Kubik et al 2007) or (Frankland et al 2004;Maviel et al 2004;Kubik et al 2007;Mamiya et al 2009). …”

Section: Discussionmentioning

confidence: 99%

Localization of molecular correlates of memory consolidation to buccal ganglia mechanoafferent neurons after learning that food is inedible in Aplysia

et al. 2012

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Training paradigms affecting Aplysia withdrawal reflexes cause changes in gene expression leading to long-term memory formation in primary mechanoafferents that initiate withdrawal. Similar mechanoafferents are also found in the buccal ganglia that control feeding behavior, raising the possibility that these mechanoafferents are a locus of memory formation after a training paradigm affecting feeding. Buccal ganglia mechanoafferent neurons expressed increases in mRNA expression for the transcription factor ApC/EBP, and for the growth factor sensorin-A, within the first 2 h after training with an inedible food. No increases in expression were detected in the rest of the buccal ganglia. Increased ApC/EBP expression was not elicited by food and feeding responses not causing long-term memory. Increased ApC/EBP expression was directly related to a measure of the efficacy of training in causing long-term memory, suggesting that ApC/EBP expression is necessary for the expression of aspects of long-term memory. In behaving animals, memory is expressed as a decrease in the likelihood to respond to food, and a decrease in the amplitude of protraction, the first phase of consummatory feeding behaviors.To determine how changes in the properties of mechanoafferents could cause learned changes in feeding behavior, synaptic contacts were mapped from the mechanoafferents to the B31/B32 neurons, which have a key role in initiating consummatory behaviors and also control protractions. Many mechanoafferents monosynaptically and polysynaptically connect with B31/B32. Monosynaptic connections were complex combinations of fast and slow excitation and/or inhibition. Changes in the response of B31/B32 to stimuli sensed by the mechanoafferent could underlie aspects of long-term memory expression.[Supplemental material is available for this article.]In a number of learning paradigms affecting Aplysia withdrawal reflexes, the connection from mechanoafferent neurons to effectors has been a major focus of research on how neural plasticity is translated into behavioral change (Byrne and

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Requirement of New Protein Synthesis of a Transcription Factor for Memory Consolidation: Paradoxical Changes in mRNA and Protein Levels of C/EBP

Cited by 52 publications

References 46 publications

One-trial conditioned taste aversion inLymnaea: good and poor performers in long-term memory acquisition

One-trial conditioned taste aversion inLymnaea: good and poor performers in long-term memory acquisition

Training with inedible food in Aplysia causes expression of C/EBP in the buccal but not cerebral ganglion

Localization of molecular correlates of memory consolidation to buccal ganglia mechanoafferent neurons after learning that food is inedible in Aplysia

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