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Roles of NO signaling in long-term memory formation in visual learning in an insect.

Matsumoto Y, Hirashima D, Terao K, Mizunami M - PLoS ONE (2013)

Bottom Line: In this study, we examined the possible contribution of NO-cGMP signaling and cAMP signaling to LTM formation in visual pattern learning in crickets.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.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Life Science, Hokkaido University, Sapporo, Japan.

ABSTRACT
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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Related in: MedlinePlus

Effects of 8-br-cAMP on visual LTM formation.At 20 min prior to 4-trial visual conditioning, two groups of animals were each injected with 3 μl of saline or saline containing 20 μl or 200 μl 8-br-cAMP. Relative preference between the rewarded pattern and control pattern was tested before and at 1 day after conditioning. PIs for rewarded pattern before (white bars) and after (grey bars) training are shown as box plots, and the results of statistical comparison between them are indicated (** p<0.01, NS p>0.05, WCX test).
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pone-0068538-g006: Effects of 8-br-cAMP on visual LTM formation.At 20 min prior to 4-trial visual conditioning, two groups of animals were each injected with 3 μl of saline or saline containing 20 μl or 200 μl 8-br-cAMP. Relative preference between the rewarded pattern and control pattern was tested before and at 1 day after conditioning. PIs for rewarded pattern before (white bars) and after (grey bars) training are shown as box plots, and the results of statistical comparison between them are indicated (** p<0.01, NS p>0.05, WCX test).

Mentions: We next tested whether injection of 8-br-cAMP, a membrane-permeable cAMP analogue, can facilitate visual LTM formation. Two groups of animals were each injected with 3 μl or saline containing 20 μM or 200 μM 8-br-cAMP at 20 min prior to 4-trial conditioning, and their preferences were tested before and 1 day after conditioning. The group injected with 20 μM 8-br-cAMP exhibited no significant level of 1-day retention (Figure 6, W=206, p=0.29, WCX test), as in the case of the saline-injected group (see Figure 4). In contrast, the 200 μM 8-br-cAMP-injected group exhibited a significant level of 1-day retention, (W=72, p=0.0039, WCX test), indicating that externally applied cAMP facilitates LTM formation.


Roles of NO signaling in long-term memory formation in visual learning in an insect.

Matsumoto Y, Hirashima D, Terao K, Mizunami M - PLoS ONE (2013)

Effects of 8-br-cAMP on visual LTM formation.At 20 min prior to 4-trial visual conditioning, two groups of animals were each injected with 3 μl of saline or saline containing 20 μl or 200 μl 8-br-cAMP. Relative preference between the rewarded pattern and control pattern was tested before and at 1 day after conditioning. PIs for rewarded pattern before (white bars) and after (grey bars) training are shown as box plots, and the results of statistical comparison between them are indicated (** p<0.01, NS p>0.05, WCX test).
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3722230&req=5

pone-0068538-g006: Effects of 8-br-cAMP on visual LTM formation.At 20 min prior to 4-trial visual conditioning, two groups of animals were each injected with 3 μl of saline or saline containing 20 μl or 200 μl 8-br-cAMP. Relative preference between the rewarded pattern and control pattern was tested before and at 1 day after conditioning. PIs for rewarded pattern before (white bars) and after (grey bars) training are shown as box plots, and the results of statistical comparison between them are indicated (** p<0.01, NS p>0.05, WCX test).
Mentions: We next tested whether injection of 8-br-cAMP, a membrane-permeable cAMP analogue, can facilitate visual LTM formation. Two groups of animals were each injected with 3 μl or saline containing 20 μM or 200 μM 8-br-cAMP at 20 min prior to 4-trial conditioning, and their preferences were tested before and 1 day after conditioning. The group injected with 20 μM 8-br-cAMP exhibited no significant level of 1-day retention (Figure 6, W=206, p=0.29, WCX test), as in the case of the saline-injected group (see Figure 4). In contrast, the 200 μM 8-br-cAMP-injected group exhibited a significant level of 1-day retention, (W=72, p=0.0039, WCX test), indicating that externally applied cAMP facilitates LTM formation.

Bottom Line: In this study, we examined the possible contribution of NO-cGMP signaling and cAMP signaling to LTM formation in visual pattern learning in crickets.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.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Life Science, Hokkaido University, Sapporo, Japan.

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus