Cellular and molecular analysis of associative learning and memory in Hermissenda

Crow, Terry

doi:10.1016/0166-2236(88)90138-5

Cited by 90 publications

(53 citation statements)

References 36 publications

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“…Work from several vertebrate and invertebrate model systems has revealed the involvement of neurotransmitters, their receptors, ion channels, G-proteins, adenylyl cyclase, phosphodiesterase, and protein kinases within the first few hours after an animal learns something new about its environment (Kandel et al, 1987;Crow, 1988;Madison et al, 199 I ;Tully, I99 1). By biochemical and molecular analyses, the Drosophila learning/memory genes dunce and rutabaga, in particular, were found to encode a CAMP phosphodiesterase and an adenylyl cyclase, respectively (Chen et al, 1986;Levin et al, 1992)-lending support to the notion that the basic molecular mechanisms of (some of) these early events may be evolutionarily conserved.…”

Section: Memory Through Metamorphosis In Normal and Mutant Drosophilamentioning

confidence: 99%

Memory through metamorphosis in normal and mutant Drosophila

1994

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To establish that a stable, long-lasting form of memory exists in Drosophila, we trained third-instar larvae by electroshocking them in the presence of a specific odor using a Pavlovian conditioning procedure. We show that conditioned odor avoidance produced in larvae still was present in adults 8 d later. Such memory through metamorphosis was specific to the temporal pairing of odor and shock; presentations of odors alone or shock alone did not produce a change. Thus, the memory involved associative processes. We also show that similar training of the single-gene memory mutants dunce and amnesiac did not yield any detectable learning in larvae or memory retention in adults, suggesting that these mutations interfere with long-term memory (LTM) formation even if LTM is induced independently of earlier memory retention processes.

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Section: Memory Through Metamorphosis In Normal and Mutant Drosophilamentioning

confidence: 99%

Memory through metamorphosis in normal and mutant Drosophila

1994

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“…We previously reported that one-trial in vivo conditioning produces both a short-term and a long-term enhancement of light-evoked generator potentials recorded from identified medial and lateral B photoreceptors (13). Short-term enhancement of generator potentials recorded from medial and lateral B photoreceptors is not dependent upon pairing the CS with 5-HT, whereas long-term enhancement found only in lateral B photoreceptors is dependent upon pairing the CS with 5-HT, (11,13). Pretreatment with 1 AuM anisomycin did not block the induction or the expression of enhanced generator potentials produced by light and 5-HT recorded from medial or lateral B photoreceptors 1 hr after the conditioning trial.…”

Section: Resultsmentioning

confidence: 99%

“…Recently, studies of short-and long-term synaptic facilitation of monosynaptic connections between cultured sensory and motor neurons in Aplysia revealed that inhibitors of protein or RNA synthesis blocked long-term facilitation, while leaving short-term facilitation intact (6). Studies of short-term and long-term synaptic and cellular plasticity in invertebrate nervous systems are particularly attractive since such preparations provide for the opportunity of relating biochemical and molecular changes in identified neuronal cell types to learning and memory (6)(7)(8)(9)(10)(11). The results of recent studies of Hermissenda have shown that a one-trial in vivo conditioning procedure produces a long-term change in phototactic behavior that depends upon pairing a conditioned stimulus (CS) with the direct application of serotonin (5-hydroxytryptamine, 5-HT) to the exposed nervous system of otherwise intact animals (12).…”

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confidence: 99%

“…The animals were coded so that the experimenter collecting the electrophysiological data did not know the treatment condition that a given preparation had received. The nervous systems were removed, and B photoreceptors were isolated by axotomy of the optic nerve as described (11,22). After 15 min of dark adaptation, generator potentials elicited by a 2-min light step (10 x 10-4 W/cm2 at 510 nm) were recorded from visually identified B photoreceptors in the medial and lateral position in the eye by using standard procedures for intracellular recording and light stimulation.…”

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Inhibition of protein synthesis blocks long-term enhancement of generator potentials produced by one-trial in vivo conditioning in Hermissenda.

Crow

Forrester

1990

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

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A one-trial in vivo conditionig procedure produces short-and long-term cellular changes that can be detected in identified sensory neurons ofthe pathway mediating the conditioned stimulus. The memory of the associative experience in the conditioned stimulus pathway is expressed by short-and long-term enhancement of light-evoked generator potentials recorded from identified lateral and medial type B photoreceptors within the eyes of Hermissenda. To identify mechanisms of the induction and expression of short-and long-term enhancement in identified photoreceptors, we have investigated the effects of inhibiting protein synthesis during the application of the one-trial in vivo conditioning procedure. Anisomycin (1 pLM) present during and after the conditioning trial blocked long-term enhancement without affecting the induction or expression of short-term enhancement. Application of a control compound, deacetylanisomycin (1 PzM), or delaying the application of anisomycin until 1 hr after the conditioning trial did not block either long-or short-term enhancement. These results indicate that synthesis of proteins during or shortly after training may be a critical step in the formation of long-term memory of the associative experience.Behavioral and cellular neurophysiological studies of memory have provided support for the hypothesis that protein synthesis during or shortly after an experience is a necessary step for the formation of enduring forms of memory called long-term memory (review in ref. 1). Support for the hypothesis that, for long-term memory to be formed, proteins must be synthesized is provided by learning and memory studies of vertebrates where inhibition of protein synthesis and/or RNA synthesis interferes with the formation of long-term memory while short-term memory remains relatively intact (2-5). Recently, studies of short-and long-term synaptic facilitation of monosynaptic connections between cultured sensory and motor neurons in Aplysia revealed that inhibitors of protein or RNA synthesis blocked long-term facilitation, while leaving short-term facilitation intact (6). Studies of short-term and long-term synaptic and cellular plasticity in invertebrate nervous systems are particularly attractive since such preparations provide for the opportunity of relating biochemical and molecular changes in identified neuronal cell types to learning and memory (6-11). The results of recent studies of Hermissenda have shown that a one-trial in vivo conditioning procedure produces a long-term change in phototactic behavior that depends upon pairing a conditioned stimulus (CS) with the direct application of serotonin (5-hydroxytryptamine, 5-HT) to the exposed nervous system of otherwise intact animals (12). One site for cellular changes that may contribute to the long-term behavioral modification is the sensory pathway mediating the CS. We recently reported that one-trial in vivo conditioning produces both a short-term nonassociative enhancement and a long-term associative enhancement of generator potenti...

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“…It is therefore possible to correlate behavior with specific electrophysiological, neurochemical, and structural cytological changes (Alkon and Fuortes, 1972;Alkon, 1984;Crow, 1988Crow, , 2004Alkon and Nelson, 1990;Alkon et al, , 1998Kawai et al, 2002;Nelson et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Bryostatin Enhancement of Memory inHermissenda

Kuzirian

Epstein

Gagliardi

et al. 2006

The Biological Bulletin

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Abstract. Bryostatin, a potent agonist of protein kinase C (PKC), when administered to Hermissenda was found to affect acquisition of an associative learning paradigm. Low bryostatin concentrations (0.1 to 0.5 ng/ml) enhanced memory acquisition, while concentrations higher than 1.0 ng/ml down-regulated the pathway and no recall of the associative training was exhibited. The extent of enhancement depended upon the conditioning regime used and the memory stage normally fostered by that regime. The effects of two training events (TEs) with paired conditioned and unconditioned stimuli, which standardly evoked only short-term memory (STM) lasting 7 min, were-when bryostatin was added concurrently-enhanced to a long-term memory (LTM) that lasted about 20 h. The effects of both 4-and 6-paired TEs (which by themselves did not generate LTM), were also enhanced by bryostatin to induce a consolidated memory (CM) that lasted at least 5 days. The standard positive 9-TE regime typically produced a CM lasting at least 6 days. Low concentrations of bryostatin (Ͻ0.5 ng/ml) elicited no demonstrable enhancement of CM from 9-TEs. However, animals exposed to bryostatin concentrations higher than 1.0 ng/ml exhibited no behavioral learning.Sharp-electrode intracellular recordings of type-B photoreceptors in the eyes from animals conditioned in vivo with bryostatin revealed changes in input resistance and an enhanced long-lasting depolarization (LLD) in response to light. Likewise, quantitative immunocytochemical measurements using an antibody specific for the PKC-activated Ca 2ϩ /GTP-binding protein calexcitin showed enhanced antibody labeling with bryostatin.Animals exposed to the PKC inhibitor bisindolylmaleimide-XI (Ro-32-0432) administered by immersion prior to 9-TE conditioning showed no training-induced changes with or without bryostatin exposure. However, if animals received bryostatin before Ro-32, the enhanced acquisition and demonstrated recall still occurred. Therefore, pathways responsible for the enhancement effects induced by bryostatin were putatively mediated by PKC.Overall, the data indicated that PKC activation occurred and calexcitin levels were raised during the acquisition phases of associative conditioning and memory initiation, and subsequently returned to baseline levels within 24 and 48 h, respectively. Therefore, the protracted recall measured by the testing regime used was probably due to bryostatininduced changes during the acquisition and facilitated storage of memory, and not necessarily to enhanced recall of the stored memory when tested many days after training.

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Cellular and molecular analysis of associative learning and memory in Hermissenda

Cited by 90 publications

References 36 publications

Memory through metamorphosis in normal and mutant Drosophila

Memory through metamorphosis in normal and mutant Drosophila

Inhibition of protein synthesis blocks long-term enhancement of generator potentials produced by one-trial in vivo conditioning in Hermissenda.

Bryostatin Enhancement of Memory inHermissenda

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