Circadian modulation of long-term sensitization in
            <i>Aplysia</i>

Fernandez, Raymond; Lyons, Lisa C.; Levenson, Jonathan M.; Khabour, Omar F.; Eskin, Arnold

doi:10.1073/pnas.2336172100

Cited by 58 publications

(100 citation statements)

References 49 publications

(51 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Coupled with the fact that animals trained at CT 2 were unable to recall a memory after only 5-30 min, these results suggest that the inability of animals to perform when trained at CT 2 was due to an inability to form new memories at this circadian phase and focus attention on the earliest stages of olfactory memory formation, rather than retention or memory retrieval. This notion is generally consistent with the recent discovery in mice that early long-term potentiation in the hippocampus is regulated by the circadian system (30), but is contrasted in Aplysia, where the circadian system modulates long-term memory, but short-term memory appears to be independent of the circadian phase (6,8).…”

Section: Memory Acquisition Vs Memory Retrievalsupporting

confidence: 90%

“…In some instances, the circadian phase may function as a context for learning (time stamping) so that recall and performance are better at 24-h intervals after learning (1)(2)(3)(4). In other cases, performance may be modulated by the circadian phase independent of the phase of learning (5), and there have been several recent reports that memory acquisition or consolidation may depend on the circadian phase of training in mollusks (6)(7)(8), rodents (9,10), and humans (11). Finally, there have been reports that disruption of the circadian system by phase shifting (jet lag) can impair memory (12,13).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Circadian regulation of insect olfactory learning

Decker

McConnaughey

Page

2007

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Olfactory learning in insects has been used extensively for studies on the neurobiology, genetics, and molecular biology of learning and memory. We show here that the ability of the cockroach Leucophaea maderae to acquire olfactory memories is regulated by the circadian system. We investigated the effect of training and testing at different circadian phases on performance in an odordiscrimination test administered 30 min after training (short-term memory) or 48 h after training (long-term memory). When odor preference was tested by allowing animals to choose between two odors (peppermint and vanilla), untrained cockroaches showed a clear preference for vanilla at all circadian phases, indicating that there was no circadian modulation of initial odor preference or ability to discriminate between odors. After differential conditioning, in which peppermint odor was associated with a positive unconditioned stimulus of sucrose solution and vanilla odor was associated with a negative unconditioned stimulus of saline solution, cockroaches conditioned in the early subjective night showed a strong preference for peppermint and retained the memory for at least 2 days. Animals trained and tested at other circadian phases showed significant deficits in performance for both short-and long-term memory. Performance depended on the circadian time (CT) of training, not the CT of testing, and results indicate that memory acquisition rather than retention or recall is modulated by the circadian system. The data suggest that the circadian system can have profound effects on olfactory learning in insects.biological rhythms ͉ cockroach ͉ differential conditioning ͉ memory I n view of the widespread effects of circadian regulation on behavior and physiology, the possibility that learning and memory processes may be subject to modulation by the circadian system has long been recognized (1). Studies on this problem have suggested that the influence of the circadian system may take several forms. In some instances, the circadian phase may function as a context for learning (time stamping) so that recall and performance are better at 24-h intervals after learning (1-4). In other cases, performance may be modulated by the circadian phase independent of the phase of learning (5), and there have been several recent reports that memory acquisition or consolidation may depend on the circadian phase of training in mollusks (6-8), rodents (9, 10), and humans (11). Finally, there have been reports that disruption of the circadian system by phase shifting (jet lag) can impair memory (12, 13). Although these studies suggest that the circadian system may have widespread effects on various aspects of learning and memory, including acquisition, retention, and recall, there is virtually no information on the mechanisms by which the circadian system regulates these processes.Olfactory learning is an excellent model for exploration of the neural basis of learning and memory because of the remarkable similarity in the organization of olfactory systems acr...

show abstract

Section: Memory Acquisition Vs Memory Retrievalsupporting

confidence: 90%

mentioning

confidence: 99%

Circadian regulation of insect olfactory learning

Decker

McConnaughey

Page

2007

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…Long-term sensitization is modulated by circadian rhythm in Aplysia (Fernandez et al 2003), and 5-HT levels follow a light-dark rhythm in hemolymph (Levenson et al 1999). In contrast, in continuous darkness, systemic 5-HT levels are constant but the long-term sensitization rhythm remains (Fernandez et al 2003).…”

Section: Discussionmentioning

confidence: 98%

Systemic serotonin sulfate in opisthobranch mollusks

Stuart¹,

Ebaugh²,

Copes³

et al. 2004

Journal of Neurochemistry

View full text Add to dashboard Cite

Serotonin (5-hydroxytryptamine, 5-HT) is a ubiquitous modulatory neurotransmitter with roles as a neurohormone and neurotransmitter. However, few studies have been performed characterizing this molecule and its related metabolites in circulating fluids. Here, we demonstrate native 5-HT sulfate, but much lower levels of 5-HT, in hemolymph of the marine mollusk Pleurobranchaea californica. The metabolite 5-HT sulfate forms from 5-HT uptake and metabolism in central ganglia of Aplysia californica and in the visceral nerve and eye of Pleurobranchaea, but not in hemolymph itself. In addition, 5-hydroxyindole acetic acid (5-HIAA), while not detected in hemolymph, forms in higher quantities than does 5-HT sulfate in the eye and visceral nerve, and c-glu-5-HT is also observed in this area but never in hemolymph. As systemic 5-HT sulfate appears not to originate from the optic region or from systemic 5-HT, 5-HT sulfate likely derives from the nervous system. Circulating 5-HT sulfate is at least 10-fold higher during the light portion of a 12 : 12-h light/dark cycle than during the dark portion (p < 0.0007), but there is no obvious trend for free systemic tryptophan (Trp) (p > 0.3) in Pleurobranchaea. 5-HT in mollusks is associated with general arousal state; thus, diurnal systemic changes in a 5-HT catabolite may reflect a regulatory role for indole catabolism in behavioral rhythms. Keywords: capillary electrophoresis, hemolymph, marine mollusk, serotonin, sulfation. Serotonin (5-hydroxytryptamine, 5-HT) is a biogenic amine responsible for a variety of tasks in the nervous system. For instance, 5-HT is implicated in learning and memory in the central nervous system (CNS) and emesis and peristaltic reflex in the enteric nervous system (ENS) (Bartsch et al. 2000;Buhot et al. 2000;Endo et al. 2000). Several organs serve as targets for 5-HT, but the fate of 5-HT in target tissues, let alone the physiological effects of the resulting metabolites, has not been fully ascertained. Knowledge of the products of transformed 5-HT, as well as their distribution patterns, will assist in illuminating the processes leading to impaired neurotransmission and eventually aid in designing compounds that could potentially inhibit disease in neural and surrounding tissues.Marine mollusks present an excellent model for the study of the nervous system because of their large cell somata and well-characterized neural networks. In gastropod mollusks, 5-HT is involved in many neurophysiological processes, including sensitization and facilitation of withdrawal reflexes (Hawkins et al. 1993), feeding behavior (Gillette and Davis 1977) and locomotion (McPherson and Blankenship 1991). However, 5-HT-related metabolites have received considerably less attention.Our laboratory recently demonstrated that 5-HT metabolism in Aplysia californica involves sulfation and c-glutamylation with trace amounts of monoamine oxidase activity present in the form of 5-hydroxyindole acetic acid (5-HIAA) (Stuart et al. 2003). In particular, 5-HT sulfate is present ...

show abstract

“…LTS testing and training were done as described previously (Scholz and Byrne, 1987;Cleary et al, 1998;Levenson et al, 2000b;Fernandez et al, 2003). Briefly, the tail siphon withdrawal response was elicited by electrical stimulation through a pair of electrodes implanted in either side of the tail.…”

Section: Methodsmentioning

confidence: 99%

Coregulation of Glutamate Uptake and Long-Term Sensitization inAplysia

Khabour¹,

Levenson²,

Lyons³

et al. 2004

J. Neurosci.

View full text Add to dashboard Cite

In Aplysia, long-term facilitation (LTF) at sensorimotor synapses of the pleural-pedal ganglia is mediated by an increase in the release of a neurotransmitter, which appears to be glutamate. Glutamate uptake also is increased in sensory neurons 24 hr after the induction of long-term sensitization (Levenson et al., 2000b). The present study investigated whether the same signaling pathways were involved in the long-term increase in glutamate uptake as in the induction of LTF. Thus, roles for cAMP, PKA (cAMP-dependent protein kinase), MAPK (mitogen-activated protein kinase), and tyrosine kinase in the regulation of glutamate uptake were tested. We found that 5-HT increased cAMP and activated PKA in sensory neurons. Exposure of pleural-pedal ganglia to analogs of cAMP or forskolin increased glutamate uptake 24 hr after treatments. Inhibitors of PKA (KT5720), MAPK (U0126 and PD98059), and tyrosine kinase (genistein) blocked the long-term increase in glutamate uptake produced by 5-HT. In addition, bpV, a tyrosine phosphatase inhibitor, facilitated the ability of subthreshold levels of 5-HT to increase glutamate uptake. Inhibition of PKC, which is not involved in LTF, had no effect on the long-term increase in glutamate uptake produced by 5-HT. Furthermore, activation of PKC by phorbol-12,13-dibutyrate did not produce long-term changes in glutamate uptake. The results demonstrate that the same constellation of second messengers and kinases is involved in the long-term regulation of both glutamate release and glutamate uptake. These similarities in signaling pathways suggest that regulation of glutamate release and uptake during formation of long-term memory are coordinated through coregulation of these two processes.

show abstract

Circadian modulation of long-term sensitization in Aplysia

Cited by 58 publications

References 49 publications

Circadian regulation of insect olfactory learning

Circadian regulation of insect olfactory learning

Systemic serotonin sulfate in opisthobranch mollusks

Coregulation of Glutamate Uptake and Long-Term Sensitization inAplysia

Contact Info

Product

Resources

About