Invertebrate Learning and Memory: From Behavior to Molecules

Carew, Thomas; Sahley, Christie L.

doi:10.1146/annurev.ne.09.030186.002251

Cited by 387 publications

(124 citation statements)

References 148 publications

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“…In a typical experiment, high K+ stimulations were presented every 5 min until over half of the cellular response had been lost through habituation. The cells were then allowed to rest for 20 min, after which a significant restoration in the response was found. Subsequent repetitive stimulation led to further habituation.…”

Section: Resultsmentioning

confidence: 99%

Habituation in the single cell: diminished secretion of norepinephrine with repetitive depolarization of PC12 cells.

McFadden

Koshland²

1990

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

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Neuronally (7), and take on many of the biochemical traits of sympathetic noradrenergic neurons (5). Membrane depolarization, mediated by raising the K+ concentration in the medium, evokes neurosecretion of catecholamines from these cells (8). Ca2+ influx through voltage-gated channels is the proposed second messenger for neurosecretion (9). Phorbol ester treatment increases secretion by PC12 cells (10), presumably through the activation of protein kinase C (11).To test whether neuronally differentiated PC12 cells would be an appropriate model system for habituation and memory, cells were presented with repetitive membrane depolarization, and their neurotransmitter secretion was measured. The resulting cellular behavior satisfies several of the criteria that have been used to classify habituation in organisms (12). The effects of a Ca2+-channel agonist and protein kinase C activation by phorbol esters were also tested. The results reveal that habituation occurs within single cells and is affected by important second messenger systems.EXPERIMENTAL PROCEDURES Cells and Media. The rat pheochromocytoma cell line PC12 was obtained from the American Type Culture Collection and was cultured on dextran beads in the presence of nerve growth factor for 7-10 days. Culture medium was formulated as RPMI 1640 growth medium/10% heat-inactivated horse serum (56°, 30 min)/5% fetal bovine serum/penicillin (20 units ml-1)/streptomycin (20 units ml-1)/20 mM sodium Hepes, pH 7.4 (6). Test media for secretion measurements were formulated as reported (8) Approximately half of the radiolabel in the medium was taken up by the cells in this time and was evidently stored in secretory granules (13, 14) because we found that >80% of the intracellular radiolabel would sediment after lysis of the cells with digitonin. The cell-covered beads (106 cells; 5 x 104 beads; 4 x 106 dpm) were then transferred to a perfused cell-chamber constructed from a plastic-syringe barrel (0.15-ml internal volume) and with a glass-fiber filter at its outlet.[3H]Norepinephrine Secretion Measurements. Cellular secretion of [3H]norepinephrine was measured by a method adapted from previous studies (15). Medium was delivered to the cell chamber by a peristaltic pump (0.28 ml-min-1), the stream of medium exiting the cell chamber was mixed with a stream of scintillation fluid (2.2 ml-min-'), and the mixed streams then entered a flow-through scintillation detector (Flo-One Beta; Radiomatic Instruments and Chemical, Tampa, FL). The number of cpm of radioactivity passing through the scintillation counter was updated and recorded every 0.1 min. Secretion was evoked by switching the medium coming into the cell chamber to high K+. The total amount of radiolabel present in the cells was determined after lysis of the cells by detergent at the end of each experiment with 1% (vol/vol) Triton X-100. During 1-to 3-hr experiments, between 10 and 30% of the initial cellular radiolabel was released, depending on the number of stimuAbbreviation: PMA, 4,8-phorbol 12-myristate ...

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Section: Resultsmentioning

confidence: 99%

Habituation in the single cell: diminished secretion of norepinephrine with repetitive depolarization of PC12 cells.

McFadden

Koshland²

1990

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

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“…The results of our study demonstrate for the first time that a successful conspecific mating experience enhances a D. melanogaster male’s ability to compete for new mates, and we show that the male’s success is linked to changes in courtship behavior. Ability to survive and successfully face changing environments is often accompanied by variation in behavioral tactics [39], [40], [41], and such changes in behavior due to experience meet common definitions of learning [42], [43]. Sexual experience provides animals the opportunity to hone their skills and improve courtship towards future mates, gaining advantage over naïve individuals who lack such experience.…”

Section: Discussionmentioning

confidence: 99%

Sexual Experience Enhances Drosophila melanogaster Male Mating Behavior and Success

et al. 2014

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Competition for mates is a wide-spread phenomenon affecting individual reproductive success. The ability of animals to adjust their behaviors in response to changing social environment is important and well documented. Drosophila melanogaster males compete with one another for matings with females and modify their reproductive behaviors based on prior social interactions. However, it remains to be determined how male social experience that culminates in mating with a female impacts subsequent male reproductive behaviors and mating success. Here we show that sexual experience enhances future mating success. Previously mated D. melanogaster males adjust their courtship behaviors and out-compete sexually inexperienced males for copulations. Interestingly, courtship experience alone is not sufficient in providing this competitive advantage, indicating that copulation plays a role in reinforcing this social learning. We also show that females use their sense of hearing to preferentially mate with experienced males when given a choice. Our results demonstrate the ability of previously mated males to learn from their positive sexual experiences and adjust their behaviors to gain a mating advantage. These experienced-based changes in behavior reveal strategies that animals likely use to increase their fecundity in natural competitive environments.

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“…The study of memory, therefore, has benefited from the attempt to combine behavioral with reductionist approaches designed to analyze the neurobiological mechanisms of memory in cellular terms (50). Reductionist studies have been particularly effective with simple vertebrate behaviors and several tractable, higher invertebrate systems (2)(3)(4)55). Of the several invertebrate systems, Aplysia and Drosophila have been particularly informative, because memory in these animals has been shown to have both short-and long-term components (56).…”

Section: Potential Behavioral Significance Of Different Forms Of Ltfmentioning

confidence: 99%

“…he gill-and siphon-withdrawal reflex of Aplysia has proven a useful model system for studying the cellular and molecular basis of simple forms of learning and memory (1)(2)(3)(4). The molecular mechanisms of memory storage have been particularly well studied in the context of sensitization, an elementary form of nonassociative learning in which an animal learns to strengthen its reflex responses to previously neutral stimuli after the presentation of an aversive stimulus.…”

mentioning

confidence: 99%

A novel function for serotonin-mediated short-term facilitation in Aplysia : Conversion of a transient, cell-wide homosynaptic Hebbian plasticity into a persistent, protein synthesis-independent synapse-specific enhancement

Bailey

Giustetto

Zhu

et al. 2000

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

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Studies of sensitization and classical conditioning of the gill-withdrawal reflex in Aplysia have shown that the synaptic connections between identified glutamatergic sensory neurons and motor neurons can be enhanced in one of two ways: by a heterosynaptic (modulatory input-dependent) mechanism that gives rise with repetition to long-term facilitation and by a homosynaptic (activitydependent) mechanism that gives rise with repetition to a facilitation that is partially blocked by 2-amino-5-phosphonovaleric acid and by injection of 1,2-bis(2-aminophenoxy)ethane-N,N,N,N-tetraacetate (BAPTA) into the postsynaptic cell and is similar to long-term potentiation in the hippocampus. We here have examined how these two forms of facilitation interact at the level of an individual synaptic connection by using a culture preparation consisting of a single bifurcated sensory neuron that forms independent synaptic contacts with each of two spatially separated motor neurons. We find that the homosynaptic facilitation produced by a train of action potentials is cell wide and is evident at all of the terminals of the sensory neuron. By contrast, the heterosynaptic facilitation mediated by the modulatory transmitter serotonin (5-HT) can operate at the level of a single synapse. Homosynaptic activation gives rise to only a transient facilitation lasting a few hours, even when repeated in a spaced manner. The heterosynaptic facilitation produced by a single pulse of 5-HT, applied to one terminal of the sensory neuron, also lasts only minutes. However, when one or more homosynaptic trains of spike activity are paired with even a single pulse of 5-HT applied to one of the two branches of the sensory neuron, the combined actions lead to a selective enhancement in synaptic strength only at the 5-HTtreated branch that now lasts more than a day, and thus amplifies, by more than 20-fold, the duration of the individually produced homoand heterosynaptic facilitation. This form of synapse-specific facilitation has unusual long-term properties. It does not require protein synthesis, nor is it accompanied by synaptic growth. T he gill-and siphon-withdrawal reflex of Aplysia has proven a useful model system for studying the cellular and molecular basis of simple forms of learning and memory (1-4). The molecular mechanisms of memory storage have been particularly well studied in the context of sensitization, an elementary form of nonassociative learning in which an animal learns to strengthen its reflex responses to previously neutral stimuli after the presentation of an aversive stimulus. As is the case for other defensive withdrawal reflexes, the behavioral memory for sensitization of the gill-and siphon-withdrawal reflex is graded, and the duration of the memory is a function of the number of training trials. A single stimulus to the tail gives rise to short-term sensitization lasting minutes to hours. Repetition of the stimulus produces long-term behavioral sensitization that can last days to weeks (5, 6). The memory for both the short-and lo...

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Invertebrate Learning and Memory: From Behavior to Molecules

Cited by 387 publications

References 148 publications

Habituation in the single cell: diminished secretion of norepinephrine with repetitive depolarization of PC12 cells.

Habituation in the single cell: diminished secretion of norepinephrine with repetitive depolarization of PC12 cells.

Sexual Experience Enhances Drosophila melanogaster Male Mating Behavior and Success

A novel function for serotonin-mediated short-term facilitation in Aplysia : Conversion of a transient, cell-wide homosynaptic Hebbian plasticity into a persistent, protein synthesis-independent synapse-specific enhancement

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