Participation of NO signaling in formation of long-term memory in salivary conditioning of the cockroach

Matsumoto, Chihiro Sato; Kuramochi, Tomokazu; Matsumoto, Y.; Watanabe, Hidehiro; Nishino, Hiroshi; Mizunami, Makoto

doi:10.1016/j.neulet.2013.01.010

Cited by 13 publications

(15 citation statements)

References 31 publications

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“…Much evidence has accumulated to show that nitric oxide (NO) is an important neurotransmitter and neuromodulator in both vertebrates and invertebrates (Jacklet, ; Muller, ; Fedele & Raiteri, ; Katzoff et al ., ; Eisenhardt & Menzel, ). An increasing number of studies also indicate that the NO–cyclic guanosine monophosphate (cGMP) pathway is involved in associative memory formation (Hawkins et al ., ; Rose, ; Schweighofer & Ferriol, ; Kemenes et al ., ; Matsumoto et al ., ). In the terrestrial snail Helix , it was shown (Gainutdinova et al ., ) that the protein synthesis blocker anisomycin (ANI) impairs the context memory if injected immediately after a ‘reminding’ session.…”

Section: Introductionmentioning

confidence: 97%

Nitric oxide is necessary for labilization of a consolidated context memory during reconsolidation in terrestrial snails

Balaban

Roshchin

Timoshenko

et al. 2014

Eur J of Neuroscience

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Nitric oxide (NO) is known to be involved in associative memory formation. We investigated the influence of blocking NO function on the reconsolidation of context memory in terrestrial snails (Helix lucorum L.). After a 10 day session of electric shocks in one context only, context memory in snails was observed in test sessions as the significant difference of amplitudes of withdrawal responses to tactile stimuli in two different contexts. After a 1 day rest, a session of 'reminding' was performed, preceded by injection in different groups of the snails with either vehicle or combination of the protein synthesis blocker anisomycin (ANI) with one of the following drugs: the NO scavenger carboxy-PTIO, the NO-synthase inhibitors N-omega-nitro-L-arginin, nitroindazole and NG-nitro-L-arginine methyl ester hydrochloride, or the NO donor S-nitroso-N-acetyl-DL-penicillamine. Testing the context memory at different time intervals after the reminder under ANI injection showed that the context memory was impaired at 24 h and later, whereas the reminder under combined injection of ANI and each of the NO-synthase inhibitors used or the NO scavenger showed no impairment of long-term context memory. Injection of the NO donor S-nitroso-N-acetyl-DL-penicillamine with or without reminder had no effect on context memory. The results obtained demonstrated that NO is necessary for labilization of a consolidated context memory.

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Section: Introductionmentioning

confidence: 97%

Nitric oxide is necessary for labilization of a consolidated context memory during reconsolidation in terrestrial snails

Balaban

Roshchin

Timoshenko

et al. 2014

Eur J of Neuroscience

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“…The CREB leads to transcription and translation of synaptic proteins necessary to elevate efficacy of synaptic transmission that underlies LTM [23]. The NO/cGMP system also plays critical roles in LTM formation in olfactory learning in crickets [24], [25], honey bees [26], [27] and cockroaches [28] and in visual learning in crickets [29]. In crickets, results of our pharmacological studies suggested that cAMP signaling is a downstream target of NO/cGMP signaling, cyclic nucleotide-gated (CNG) channel and Ca 2+ /CaM signaling [24], [25], which provides a solid basis for further studies on signaling cascades underlying LTM formation.…”

Section: Introductionmentioning

confidence: 99%

Roles of Calcium/Calmodulin-Dependent Kinase II in Long-Term Memory Formation in Crickets

et al. 2014

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Ca2+/calmodulin (CaM)-dependent protein kinase II (CaMKII) is a key molecule in many systems of learning and memory in vertebrates, but roles of CaMKII in invertebrates have not been characterized in detail. We have suggested that serial activation of NO/cGMP signaling, cyclic nucleotide-gated channel, Ca2+/CaM and cAMP signaling participates in long-term memory (LTM) formation in olfactory conditioning in crickets, and here we show participation of CaMKII in LTM formation and propose its site of action in the biochemical cascades. Crickets subjected to 3-trial conditioning to associate an odor with reward exhibited memory that lasts for a few days, which is characterized as protein synthesis-dependent LTM. In contrast, animals subjected to 1-trial conditioning exhibited memory that lasts for only several hours (mid-term memory, MTM). Injection of a CaMKII inhibitor prior to 3-trial conditioning impaired 1-day memory retention but not 1-hour memory retention, suggesting that CaMKII participates in LTM formation but not in MTM formation. Animals injected with a cGMP analogue, calcium ionophore or cAMP analogue prior to 1-trial conditioning exhibited 1-day retention, and co-injection of a CaMKII inhibitor impaired induction of LTM by the cGMP analogue or that by the calcium ionophore but not that by the cAMP analogue, suggesting that CaMKII is downstream of cGMP production and Ca2+ influx and upstream of cAMP production in biochemical cascades for LTM formation. Animals injected with an adenylyl cyclase (AC) activator prior to 1-trial conditioning exhibited 1-day retention. Interestingly, a CaMKII inhibitor impaired LTM induction by the AC activator, although AC is expected to be a downstream target of CaMKII. The results suggest that CaMKII interacts with AC to facilitate cAMP production for LTM formation. We propose that CaMKII serves as a key molecule for interplay between Ca2+ signaling and cAMP signaling for LTM formation, a new role of CaMKII in learning and memory.

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“…Electrophysiological techniques have been applied to the study of learning mechanisms in some invertebrates [39][40][41][42][43][44][45][46][47]. However, neurophysiological mechanisms responsible for their brain functions remain to be clarified at the level of identifiable nerve cells in the future chiefly because of experimental difficulties in recording their activities from freely behaving animals.…”

Section: Introductionmentioning

confidence: 99%

Discrimination learning with light stimuli in restrained American lobster

Tomina

Takahata

2012

Behavioural Brain Research

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Operant discrimination learning has been extensively utilized in the study on the perceptual ability of animals and their higher-order brain functions. We tested in this study whether American lobster Homarus americanus, which was previously found to possess ability of operant learning with claw gripping, could be trained to discriminate light stimuli of different intensities. For the current purpose, we newly developed a PC-controlled operant chamber that allowed the animal under a body-fixed condition to perform operant reward learning with claw gripping. Lobsters were first reinforced when they gripped the sensor bar upon presentation of a light cue. Then they were trained to grip the bar only when the light stimulus of a specific intensity was presented to obtain food reward while the stimuli of three different intensities including the reinforced one were presented in a random order. Finally, they were re-trained to grip the bar only when the light stimulus of another intensity that was not rewarded in the preceding training to obtain food while other intensities including the one that was rewarded previously were not rewarded any more. In these training procedures, the operant behavior occurred more frequently in response to the rewarded cue than to the non-rewarded one. The action latency for the reinforced stimuli showed a significant decrease in the course of training.These data demonstrate that lobsters can be trained with the light cues of different intensity as discriminative stimuli under a restrained condition that would allow application of electrophysiological techniques to the behaving subjects.-3-

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Participation of NO signaling in formation of long-term memory in salivary conditioning of the cockroach

Cited by 13 publications

References 31 publications

Nitric oxide is necessary for labilization of a consolidated context memory during reconsolidation in terrestrial snails

Nitric oxide is necessary for labilization of a consolidated context memory during reconsolidation in terrestrial snails

Roles of Calcium/Calmodulin-Dependent Kinase II in Long-Term Memory Formation in Crickets

Discrimination learning with light stimuli in restrained American lobster

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