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...

Full description

Bibliographic Details
Main Authors: Yukihisa Matsumoto, Daisuke Hirashima, Kanta Terao, Makoto Mizunami
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3722230?pdf=render
id doaj-82d7ee15f0fc4dd69237790d379d3d1f
record_format Article
spelling doaj-82d7ee15f0fc4dd69237790d379d3d1f2020-11-25T01:26:06ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0187e6853810.1371/journal.pone.0068538Roles of NO signaling in long-term memory formation in visual learning in an insect.Yukihisa MatsumotoDaisuke HirashimaKanta TeraoMakoto MizunamiMany 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.http://europepmc.org/articles/PMC3722230?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Yukihisa Matsumoto
Daisuke Hirashima
Kanta Terao
Makoto Mizunami
spellingShingle Yukihisa Matsumoto
Daisuke Hirashima
Kanta Terao
Makoto Mizunami
Roles of NO signaling in long-term memory formation in visual learning in an insect.
PLoS ONE
author_facet Yukihisa Matsumoto
Daisuke Hirashima
Kanta Terao
Makoto Mizunami
author_sort Yukihisa Matsumoto
title 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_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_sort roles of no signaling in long-term memory formation in visual learning in an insect.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
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.
url http://europepmc.org/articles/PMC3722230?pdf=render
work_keys_str_mv AT yukihisamatsumoto rolesofnosignalinginlongtermmemoryformationinvisuallearninginaninsect
AT daisukehirashima rolesofnosignalinginlongtermmemoryformationinvisuallearninginaninsect
AT kantaterao rolesofnosignalinginlongtermmemoryformationinvisuallearninginaninsect
AT makotomizunami rolesofnosignalinginlongtermmemoryformationinvisuallearninginaninsect
_version_ 1725110757039800320