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Roles of NO Signaling in Long-Term Memory Formation in Visual Learning in an Insect

Many insects exhibit excellent capability of visual learning, but the molecular and neural mechanisms are poorly understood. This is in contrast to accumulation of information on molecular and neural mechanisms of olfactory learning in insects. In olfactory learning in insects, it has been shown tha...

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Autores principales: Matsumoto, Yukihisa, Hirashima, Daisuke, Terao, Kanta, Mizunami, Makoto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3722230/
https://www.ncbi.nlm.nih.gov/pubmed/23894314
http://dx.doi.org/10.1371/journal.pone.0068538
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author Matsumoto, Yukihisa
Hirashima, Daisuke
Terao, Kanta
Mizunami, Makoto
author_facet Matsumoto, Yukihisa
Hirashima, Daisuke
Terao, Kanta
Mizunami, Makoto
author_sort Matsumoto, Yukihisa
collection PubMed
description Many insects exhibit excellent capability of visual learning, but the molecular and neural mechanisms are poorly understood. This is in contrast to accumulation of information on molecular and neural mechanisms of olfactory learning in insects. In olfactory learning in insects, it has been shown that cyclic AMP (cAMP) signaling critically participates in the formation of protein synthesis-dependent long-term memory (LTM) and, in some insects, nitric oxide (NO)-cyclic GMP (cGMP) signaling also plays roles in LTM formation. In this study, we examined the possible contribution of NO-cGMP signaling and cAMP signaling to LTM formation in visual pattern learning in crickets. Crickets that had been subjected to 8-trial conditioning to associate a visual pattern with water reward exhibited memory retention 1 day after conditioning, whereas those subjected to 4-trial conditioning exhibited 30-min memory retention but not 1-day retention. Injection of cycloheximide, a protein synthesis inhibitor, into the hemolymph prior to 8-trial conditioning blocked formation of 1-day memory, whereas it had no effect on 30-min memory formation, indicating that 1-day memory can be characterized as protein synthesis-dependent long-term memory (LTM). Injection of an inhibitor of the enzyme producing an NO or cAMP prior to 8-trial visual conditioning blocked LTM formation, whereas it had no effect on 30-min memory formation. Moreover, injection of an NO donor, cGMP analogue or cAMP analogue prior to 4-trial conditioning induced LTM. Induction of LTM by an NO donor was blocked by DDA, an inhibitor of adenylyl cyclase, an enzyme producing cAMP, but LTM induction by a cAMP analogue was not impaired by L-NAME, an inhibitor of NO synthase. The results indicate that cAMP signaling is downstream of NO signaling for visual LTM formation. We conclude that visual learning and olfactory learning share common biochemical cascades for LTM formation.
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spelling pubmed-37222302013-07-26 Roles of NO Signaling in Long-Term Memory Formation in Visual Learning in an Insect Matsumoto, Yukihisa Hirashima, Daisuke Terao, Kanta Mizunami, Makoto PLoS One Research Article Many insects exhibit excellent capability of visual learning, but the molecular and neural mechanisms are poorly understood. This is in contrast to accumulation of information on molecular and neural mechanisms of olfactory learning in insects. In olfactory learning in insects, it has been shown that cyclic AMP (cAMP) signaling critically participates in the formation of protein synthesis-dependent long-term memory (LTM) and, in some insects, nitric oxide (NO)-cyclic GMP (cGMP) signaling also plays roles in LTM formation. In this study, we examined the possible contribution of NO-cGMP signaling and cAMP signaling to LTM formation in visual pattern learning in crickets. Crickets that had been subjected to 8-trial conditioning to associate a visual pattern with water reward exhibited memory retention 1 day after conditioning, whereas those subjected to 4-trial conditioning exhibited 30-min memory retention but not 1-day retention. Injection of cycloheximide, a protein synthesis inhibitor, into the hemolymph prior to 8-trial conditioning blocked formation of 1-day memory, whereas it had no effect on 30-min memory formation, indicating that 1-day memory can be characterized as protein synthesis-dependent long-term memory (LTM). Injection of an inhibitor of the enzyme producing an NO or cAMP prior to 8-trial visual conditioning blocked LTM formation, whereas it had no effect on 30-min memory formation. Moreover, injection of an NO donor, cGMP analogue or cAMP analogue prior to 4-trial conditioning induced LTM. Induction of LTM by an NO donor was blocked by DDA, an inhibitor of adenylyl cyclase, an enzyme producing cAMP, but LTM induction by a cAMP analogue was not impaired by L-NAME, an inhibitor of NO synthase. The results indicate that cAMP signaling is downstream of NO signaling for visual LTM formation. We conclude that visual learning and olfactory learning share common biochemical cascades for LTM formation. Public Library of Science 2013-07-24 /pmc/articles/PMC3722230/ /pubmed/23894314 http://dx.doi.org/10.1371/journal.pone.0068538 Text en © 2013 Matsumoto et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Matsumoto, Yukihisa
Hirashima, Daisuke
Terao, Kanta
Mizunami, Makoto
Roles of NO Signaling in Long-Term Memory Formation in Visual Learning in an Insect
title Roles of NO Signaling in Long-Term Memory Formation in Visual Learning in an Insect
title_full Roles of NO Signaling in Long-Term Memory Formation in Visual Learning in an Insect
title_fullStr Roles of NO Signaling in Long-Term Memory Formation in Visual Learning in an Insect
title_full_unstemmed Roles of NO Signaling in Long-Term Memory Formation in Visual Learning in an Insect
title_short Roles of NO Signaling in Long-Term Memory Formation in Visual Learning in an Insect
title_sort roles of no signaling in long-term memory formation in visual learning in an insect
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3722230/
https://www.ncbi.nlm.nih.gov/pubmed/23894314
http://dx.doi.org/10.1371/journal.pone.0068538
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