Nitric Oxide Is Necessary for Multiple Memory Processes after Learning That a Food Is Inedible in<i>Aplysia</i>

Katzoff, Ayelet; Ben‐Gedalya, Tziona; Susswein, Abraham J.

doi:10.1523/jneurosci.22-21-09581.2002

Cited by 88 publications

(116 citation statements)

References 66 publications

(103 reference statements)

Supporting

Mentioning

108

Contrasting

Order By: Relevance

“…Previous studies on the roles of the NO-cGMP pathway in long-term neural plasticity in the rat hippocampus (Lu et al 1999;Lu and Hawkins 2002) and in nociceptive sensory receptors in Aplysia (Lewin and Walters 1999) suggested that the NO-cGMP pathway acts in parallel with the cAMP-PKA pathway to activate CREB, via PKG, for the formation of long-term neural plasticity. The NO-cGMP pathway plays an essential role in many systems of long-term neural and behavioral plasticity (Kendrick et al 1997;Hawkins et al 1998;Wong et al 1999;Katzoff et al 2002;Kemenes et al 2002;Lev-Ram et al 2002). It would be interesting to determine the extent by which our finding that the NO-cGMP pathway triggers LTM formation by stimulating the cAMP pathway is applicable to other systems.…”

Section: Discussionmentioning

confidence: 96%

Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory

Matsumoto

Unoki²,

Aonuma³

et al. 2006

Learn. Mem.

104

140

View full text Add to dashboard Cite

Cyclic AMP pathway plays an essential role in formation of long-term memory (LTM). In some species, the nitric oxide (NO)-cyclic GMP pathway has been found to act in parallel and complementary to the cAMP pathway for LTM formation. Here we describe a new role of the NO-cGMP pathway, namely, stimulation of the cAMP pathway to induce LTM. We have studied the signaling cascade underlying LTM formation by systematically coinjecting various "LTM-inducing" and "LTM-blocking" drugs in crickets. Multiple-trial olfactory conditioning led to LTM that lasted for several days, while memory induced by single-trial conditioning decayed away within several hours. Injection of inhibitors of the enzyme forming NO, cGMP, or cAMP into the hemolymph prior to multiple-trial conditioning blocked LTM, whereas injection of an NO donor, cGMP analog, or cAMP analog prior to single-trial conditioning induced LTM. Induction of LTM by injection of an NO donor or cGMP analog paired with single-trial conditioning was blocked by inhibitors of the cAMP pathway, but induction of LTM by a cAMP analog was unaffected by inhibitors of the NO-cGMP pathway. Inhibitors of cyclic nucleotide-gated channel (CNG channel) or calmodulin-blocked induction of LTM by cGMP analog paired with single-trial conditioning, but they did not affect induction of LTM by cAMP analog. Our findings suggest that the cAMP pathway is a downstream target of the NO-cGMP pathway for the formation of LTM, and that the CNG channel and calcium-calmodulin intervene between the NO-cGMP pathway and the cAMP pathway.In both vertebrates and invertebrates, nervous systems store information for short-term memory (STM) and long-term memory (LTM) by changing the strength of their synaptic connections (Kandel 2001). Studies in many species, including mollusca Aplysia, fruitflies Drosophila, and mice, suggest that STM storage is accompanied by transient changes in the strength of synaptic connections by covalent modifications of pre-existing proteins and that LTM storage, in contrast, is accompanied by enduring changes in synaptic strength that require transcription and translation of genes (Montarolo et al. 1986;DeZazzo and Tully 1995). In all of these species, formation of LTM requires an increase in intracellular cAMP and recruitment of the cAMP-dependent protein kinase (PKA) that phosphorylates the transcription factor, cAMP-responsive element-binding protein (CREB) (Bartsch et al. 1995;Yin et al. 1995;Abel et al. 1997).The roles of the cAMP pathway in the formation of LTM are often supplemented by other signaling pathways, most notably by the nitric oxide (NO)-cGMP signaling pathway (Lewin and Walters 1999;Lu et al. 1999). NO is a membrane-permeable molecule that functions in intercellular signaling in the brain (Garthwaite et al. 1988). In mice, NO contributes to late-phase longterm potentiation of synaptic transmission by stimulating soluble guanylate cyclase in target cells, and the resulting increase in cGMP concentration stimulates cGMP-dependent protein kinase (PKG), which acts in p...

show abstract

Section: Discussionmentioning

confidence: 96%

Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory

Matsumoto

Unoki²,

Aonuma³

et al. 2006

Learn. Mem.

104

140

View full text Add to dashboard Cite

show abstract

“…Susswein and colleagues have developed another promising composite paradigm using Aplysia feeding behavior (Susswein and Schwarz, 1983;Schwarz and Susswein, 1984, 1992Susswein et al, 1986;Schwarz et al, 1991;Chiel and Susswein, 1993;Botzer et al, 1998;Katzoff et al, 2002). Food touching the lips of Aplysia initiates biting, which causes food to enter the mouth.…”

Section: Invertebrate Composite Operant Conditioningmentioning

confidence: 99%

Cognition in Invertebrates

Menzel

Brembs

Giurfa

2007

Evolution of Nervous Systems

View full text Add to dashboard Cite

“…Additional operant-like training paradigms also affect Aplysia feeding Susswein et al 1986;Schwarz et al 1988Schwarz et al , 1991Chiel and Susswein 1993;Botzer et al 1998;Katzoff et al 2002Katzoff et al , 2006Cohen-Armon et al 2004;Lyons et al 2005). In these paradigms Aplysia are exposed to a palatable food that is difficult or impossible to consume.…”

mentioning

confidence: 99%

“…A previous report indicated that blocking nitric oxide (NO) release blocks memory after learning that food is inedible (Katzoff et al 2002). NO and histamine are released together by neuron C2, which responds to attempts to consume the food (Chiel et al 1986;Jacklet and Tieman 2004), one of the three contingent events that give rise to learning that food is inedible.…”

mentioning

confidence: 99%

“…Data that support this hypothesis include: (1) exogenous NO substituted for attempts to swallow during training with inedible food (Katzoff et al 2006);and (2) blocking NO transmission made ad libitum feeding less efficient and slowed rejection responses, presumably because animals are unable to monitor their efforts to swallow (Katzoff et al 2006). Other than affecting rejection, neither blocking NO nor treatment with a NO donor was found to affect feeding or other behaviors (Katzoff et al 2002(Katzoff et al , 2006.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible inAplysia

Katzoff¹,

Miller²,

Susswein³

2009

Learn. Mem.

Self Cite

View full text Add to dashboard Cite

Memory that food is inedible in Aplysia arises from training requiring three contingent events. Nitric oxide (NO) and histamine are released by a neuron responding to one of these events, attempts to swallow food. Since NO release during training is necessary for subsequent memory and NO substitutes for attempts to swallow, it was suggested that NO functions during training as a signal of attempts to swallow. However, it has been shown that NO may also be released in other contexts affecting feeding, raising the possibility that its role in learning is unrelated to signaling attempts to swallow. We confirmed that NO during learning signals attempts to swallow, by showing that a variety of behavioral effects on feeding of blocking or adding NO do not affect learning and memory that a food is inedible. In addition, histamine had effects similar to NO on learning that food is inedible, as expected if the transmitters are released together when animals attempt to swallow. Blocking histamine during training blocked long-term memory, and exogenous histamine substituted for attempts to swallow. NO also substituted for histamine during training. Histamine at concentrations relevant to learning activates neuron metacerebral cell (MCC). However, MCC activity is not a good monitor of attempts to swallow during training, since the neuron responds equally well to other stimuli. These findings support and extend the hypothesis that NO and histamine signal efforts to swallow during learning, acting on targets other than the MCC that specifically respond to attempts to swallow.

show abstract

Nitric Oxide Is Necessary for Multiple Memory Processes after Learning That a Food Is Inedible inAplysia

Cited by 88 publications

References 66 publications

Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory

Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory

Cognition in Invertebrates

Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible inAplysia

Contact Info

Product

Resources

About