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Cellular Studies of an Associative Mechanism for Classical Conditioning in Aplysia

Activity-dependent Presynaptic Facilitation

  • Chapter
Model Neural Networks and Behavior

Abstract

For much of this century, a central goal for both psychologists and neurobiologists has been to understand the mechanisms underlying associative learning. Of the various forms of associative learning, classical conditioning is perhaps the simplest and is thought to be the prototypical way in which an animal learns a predictive relationship (Pavlov, 1927; Kamin, 1969; Rescorla and Wagner, 1972). In classical conditioning, an animal alters its response to one stimulus as a result of the temporal pairing of this stimulus with a second event. During training, the animal comes to know that the first stimulus, called the conditioned stimulus, signals the occurrence of the second stimulus, the unconditioned stimulus. Because of its simplicity, many of the efforts to analyze cellular mechanisms of associative learning have focused on classical conditioning.

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References

  • Abrams, T. W., Carew, T. J., Hawkins, R. D., and Kandel, E. R., 1983, Aspects of the cellular mechanism of temporal specificity in conditioning in Aplysia: Preliminary evidence for Ca2+ influx as a signal of activity, Soc. Neurosci. Abstr. 9:168.

    Google Scholar 

  • Abrams, T. W., Bernier, L., Hawkins, R. D., and Kandel, E. R., 1984a, Possible roles of Ca2+ and cAMP in activity-dependent facilitation, a mechanism for associative learning in Aplysia, Soc. Neurosci. Abstr. 10:269.

    Google Scholar 

  • Abrams, T. W., Castellucci, V. F., Camardo, J. S., Kandel, E. R., and Lloyd, P. E., 1984b, Two endogenous neuropeptides modulate the gill and siphon withdrawal reflex in Aplysia by presynaptic facilitation involving cAMP-dependent closure of a serotonin-sensitive potassium channel. Proc. Natl. Acad. Sci. USA 81:7956–7960.

    Article  PubMed  CAS  Google Scholar 

  • Alkon, D. L., Lederhendler, I., and Shoukimas, J. L., 1982, Primary changes of membrane currents during retention of associative learning, Science 215:693–695.

    Article  PubMed  CAS  Google Scholar 

  • Bailey, C. H., and Chen, M., 1983, Morphological basis of long-term habituation and sensitization in Aplysia, Science 220:91–93.

    Article  PubMed  CAS  Google Scholar 

  • Bernier, L., Castellucci, V. F., Kandel, E. R., and Schwartz, J. H., 1982, Facilitatory transmitter causes a selective and prolonged increase in adenosine 3′:5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex in Aplysia, J. Neurosci. 2:1682–1691.

    PubMed  CAS  Google Scholar 

  • Brons, J. F., and Woody, C. D., 1980, Long-term changes in excitability of cortical neurons after Pav-lovian conditioning and extinction, J. Neurophysiol. 44:605–615.

    PubMed  CAS  Google Scholar 

  • Brostrom, M. A., Brostrom, C. O., Breckenridge, B. McL., and Wolff, D. J., 1978, Calcium-dependent regulation of brain adenylate cyclase, Adv. Cyclic Nucleotide Res. 9:85–99.

    PubMed  CAS  Google Scholar 

  • Brunelli, M., Castellucci, V., and Kandel, E. R., 1976, Synaptic facilitation and behavioral sensitization in Aplysia: Possible role of serotonin and cyclic AMP, Science 194:1178–1181.

    Article  PubMed  CAS  Google Scholar 

  • Byrne, J. Castellucci, V. F., and Kandel, E. R., 1974, Receptive fields and response properties of mechanoreceptor neurons innervating skin and mantle shelf of Aplysia, J. Neurophysiol. 37:1041–1064.

    PubMed  CAS  Google Scholar 

  • Byrne, J., Castellucci, V. F., and Kandel, E. R., 1978, Contribution of individual mechanoreceptor sensory neurons to defensive gill-withdrawal reflex in Aplysia, J. Neurophysiol. 41:418–431.

    PubMed  CAS  Google Scholar 

  • Carew, T. J., Walters, E. T., and Kandel, E. R., 1981, Classical conditioning in a simple withdrawal reflex in Aplysia californica, J. Neurosci. 1:1426–1437.

    PubMed  CAS  Google Scholar 

  • Carew, T. J., Hawkins, R. D., and Kandel, E. R., 1983, Differential classical conditioning of a defensive withdrawal reflex in Aplysia californica, Science 219:397–400.

    Article  PubMed  CAS  Google Scholar 

  • Carew, T. J., Abrams, T. W., Hawkins, R. D., and Kandel, E. R., 1984, A test of Hebb’s postulate at identified synapses which mediate classical conditioning in Aplysia, J. Neurosci. 4:1217–1224.

    PubMed  CAS  Google Scholar 

  • Castellucci, V. F., and Kandel, E. R., 1976, Presynaptic facilitation as a mechanism for behavioral sensitization in Aplysia, Science 194:1176–1178.

    Article  PubMed  CAS  Google Scholar 

  • Castellucci, V. F., Kandel, E. R., Schwartz, J. H., Wilson, F. D., Nairn, A. C., and Greengard, P., 1980, Intracellular injection of the catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia, Proc. Natl. Acad. Sci. U.S.A. 77:7492–7496.

    Article  PubMed  CAS  Google Scholar 

  • Castellucci, V. F., Bernier, L., Schwartz, J. H., and Kandel, E. R., 1983, Persistent activation of adenylate cyclase underlies the time course of short-term sensitization in Aplysia, Soc. Neurosci. Abstr. 9:169.

    Google Scholar 

  • Clark, G. A., McCormick, D. A., Lavond, D. G., Thompson, R. F., 1984, Effects of lesions of cerebellar nuclei on conditioned behavioral and hippocampal neuronal responses, Brain Res. 291:125–136.

    Article  PubMed  CAS  Google Scholar 

  • Crow, T. J., and Alkon, D. L., 1978, Retention of an associative behavioral change in Hermissenda, Science 201:1239–1241.

    Article  PubMed  CAS  Google Scholar 

  • Davis, W. J., Villet, J., Lee, D., Rigler, M., Gillette, R., and Prince, E., 1980, Selective and differential avoidance learning in the feeding and withdrawal behavior of Pleurobranchaea californica, J. Comp. Physiol. 138:157–165.

    Article  Google Scholar 

  • Dudai, Y., and Zvi, S., 1984, Adenylate cyclase in the Drosophila memory mutant rutabaga displays an altered Ca2+ sensitivity, Neurosci. Letters 47:119–124.

    Article  CAS  Google Scholar 

  • Gelperin, A., 1975, Rapid food-aversion learning by a terrestrial mollusk, Science 189:567–570.

    Article  PubMed  CAS  Google Scholar 

  • Glanzman, D. L., Abrams, T. W., Hawkins, R. D., and Kandel, E. R., 1984, Extracts of L29 intemeurons produce spike-broadening in sensory neurons of Aplysia, Soc. Neurosci. Abstr. 10:510.

    Google Scholar 

  • Gold, M. R., and Cohen, D. H., 1981, Modification of the discharge of vagal cardiac neurons during learned heart rate change, Science 214:345–347.

    Article  PubMed  CAS  Google Scholar 

  • Hawkins, R. D., and Abrams, T. W., 1984, Evidence that activity-dependent facilitation underlying classical conditioning in Aplysia involves modulation of the same ionic current as normal presynaptic facilitation, Soc Neurosci. Abstr. 10:268.

    Google Scholar 

  • Hawkins, R. D., Castellucci, V. F., and Kandel, E. R., 1981a, Intemeurons involved in mediation and modulation of the gill-withdrawal reflex in Aplysia. I. Identification and characterization, J. Neu-rophysiol. 45:304–314.

    CAS  Google Scholar 

  • Hawkins, R. D., Castellucci, V. F., and Kandel, E. R., 1981b, Intemeurons involved in mediation and modulation of the gill-withdrawal reflex in Aplysia. II. Identified neurons produce heterosynaptic facilitation contributing to behavioral sensitization, J. Neurophysiol. 45:315–326.

    PubMed  CAS  Google Scholar 

  • Hawkins, R. D., Abrams, T. W., Carew, T. J., and Kandel, E. R., 1983a, A cellular mechanism of classical conditioning in Aplysia: Activity-dependent amplification of presynaptic facilitation, Science 219:400–405.

    Article  PubMed  CAS  Google Scholar 

  • Hawkins, R. D., Carew, T. J., and Kandel, E. R., 1983b, Effects of interstimulus interval and contingency on classical conditioning in Aplysia, Soc. Neurosci. Abstr. 9:168.

    Google Scholar 

  • Hebb, D. O., 1949, The Organization of Behavior, New York, Wiley & Sons, Inc.

    Google Scholar 

  • Horridge, G. A., 1962, Learning of leg position by headless insects, Nature (London) 193:697–698.

    Article  CAS  Google Scholar 

  • Hoyle, G., 1980, Learning, usual natural reinforcements, in insect preparations that permit cellular neuronal analysis, J. Neurophysiol. 11:323–354.

    CAS  Google Scholar 

  • Kamin, L. J., 1969, Predictability, surprise, attention, and conditioning, in: Punishment and Aversive Behavior (B. A. Campbell and R. M. Church, eds.), Appleton-Century-Crofts, New York, pp. 279–296.

    Google Scholar 

  • Kandel, E. R., and Schwartz, J. H., 1982, Molecular biology of an elementary form of learning: Modulation of transmitter release by cyclic AMP, Science 218:433–443.

    Article  PubMed  CAS  Google Scholar 

  • Kandel, E. R., Abrams, T., Bernier, L., Carew, T. J., Hawkins, R. D., and Schwartz, J. H., 1983, Classical conditioning and sensitization share aspects of the same molecular cascade in Aplysia, Cold Spring Harbor Symp. Quant. Biol. 48:821–830.

    Article  CAS  Google Scholar 

  • Kistler, H. B., Jr., Hawkins, R. D., Koester, J., Steinbusch, H. W. M., Kandel, E. R., and Schwartz, J. H., 1985, Distribution of serotonin-immunoreactive cell bodies and processes in the abdominal ganglion of mature Aplysia, J. Neurosci. 5:72–80.

    Google Scholar 

  • Klein, M., and Kandel, E. R., 1978, Presynaptic modulation of voltage-dependent Ca2+ current: Mechanism for behavioral sensitization in Aplysia californica, Proc. Natl. Acad. Sci. U.S.A. 75:3512–3516.

    Article  PubMed  CAS  Google Scholar 

  • Klein, M., and Kandel, E. R., 1980, Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization in Aplysia, Proc. Natl. Acad. Sci. U.S.A. 77:6912–6916.

    Article  CAS  Google Scholar 

  • Klein, M., Shapiro, E., and Kandel, E. R., 1981, Synaptic plasticity and the modulation of the Ca2+ current, J. Exp. Biol. 89:117–157.

    CAS  Google Scholar 

  • Livingstone, M. S., Sziber, P. P., and Quinn, W. G., 1984, Loss of calcium/calmodulin sensitivity responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant, Cell 37:205–215.

    Article  PubMed  CAS  Google Scholar 

  • Lukowiak, K., and Sahley, C., 1981, The in vitro classical conditioning of the gill withdrawal reflex of Aplysia californica, Science 212:1516–1518.

    Article  PubMed  CAS  Google Scholar 

  • Mpitsos, G. J., and Collins, S. D., 1975, Learning: Rapid aversive conditioning in the gastropod mollusk Pleurobranchaea, Science 188:954–957.

    Article  PubMed  CAS  Google Scholar 

  • Ocorr, K. A., Walters, E. T., and Byrne, J. H., 1983, Associative conditioning analog in Aplysia tail sensory neurons selectively increases cAMP content, Soc. Neurosci. Abstr. 9:169.

    Google Scholar 

  • Pavlov, I. P., 1927, Conditioned Reflexes, Oxford University Press.

    Google Scholar 

  • Perlman, A. J., 1979, Central and peripheral control of siphon withdrawal reflex in Aplysia californica, J. Neurophysiol. 42:510–529.

    PubMed  CAS  Google Scholar 

  • Pinsker, H., Kupfermann, I., Castellucci, V., and Kandel, E. R., 1970, Habituation and dishabituation of the gill-withdrawal reflex in Aplysia, Science 167:1740–1742.

    Article  PubMed  CAS  Google Scholar 

  • Pinsker, H. M., Hening, W. A., Carew, T. J., and Kandel, E. R., 1973, Long-term sensitization of a defensive withdrawal reflex in Aplysia, Science 182:1039–1042.

    Article  PubMed  CAS  Google Scholar 

  • Quinn, W. G., Harris, W. A., and Benzer, S., 1974, Conditioned behavior in Drosophila melanogaster, Proc. Natl. Acad. Sci. U.S.A. 71:708–712.

    Article  PubMed  CAS  Google Scholar 

  • Rescorla, R. A., and Wagner, A. R., 1972, A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement, in: Classical Conditioning II: Current research and theory (A. H. Black and W. F. Prokasy, eds.), Appleton-Century-Crofts, New York, p. 64–99.

    Google Scholar 

  • Rodbell, M., 1980, The role of hormone receptors and GTP-regulatory proteins in membrane transduction, Nature (London) 284:17–22.

    Article  CAS  Google Scholar 

  • Sahley, C., Rudy, J. W., and Gelperin, A., 1981, An analysis of associative learning in a terrestrial mollusc. I. Higher-order conditioning, blocking, and a transient US pre-exposure effect, J. Comp. Physiol. 144:1–8.

    Article  Google Scholar 

  • Salter, R. S., Krinks, M. H., Klee, C. B., and Neer, E. J., 1981, Calmodulin activates the isolated catalytic unit of brain adenylate cyclase, J. Biol. Chem. 256:9830–9833.

    PubMed  CAS  Google Scholar 

  • Siegelbaum, S., Camardo, J. S., and Kandel, E. R., 1982, Serotonin and cAMP close single K+ channels in Aplysia sensory neurones, Nature (London) 299:413–417.

    Article  CAS  Google Scholar 

  • Walters, E. T., and Byrne, J. H., 1983, Associative conditioning of single sensory neurons suggests a cellular mechanism for learning, Science 219:405–408.

    Article  PubMed  CAS  Google Scholar 

  • Walters, E. T., Carew, T. J., and Kandel, E. R., 1979, Classical conditioning in Aplysia californica, Proc. Natl. Acad. Sci. USA 76:6675–6679.

    Article  PubMed  CAS  Google Scholar 

  • Walters, E. T., Byrne, J. H., Carew, T. J., and Kandel, E. R., 1983, Mechanoefferent neurons innervating the tail of Aplysia: II. Modulation by sensitizing stimulation, J. Neurophysiol. 50:1543–1559.

    PubMed  CAS  Google Scholar 

  • Woolacott, M. H., and Hoyle, G., 1977, Neural events underlying learning in insects: Changes in pacemaker, Proc. R. Soc. London Ser. B 195:395–415.

    Article  Google Scholar 

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Author information

Authors and Affiliations

  1. Center for Neurobiology and Behavior, College of Physicians and Surgeons, Columbia University, New York, New York, 10032, USA

    Thomas W. Abrams

  2. Howard Hughes Medical Institute, New York, New York, 10032, USA

    Thomas W. Abrams

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  1. Thomas W. Abrams
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Editors and Affiliations

  1. University of California, San Diego, La Jolla, California, USA

    Allen I. Selverston

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Abrams, T.W. (1985). Cellular Studies of an Associative Mechanism for Classical Conditioning in Aplysia . In: Selverston, A.I. (eds) Model Neural Networks and Behavior. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-5858-0_12

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  • DOI: https://doi.org/10.1007/978-1-4757-5858-0_12

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4757-5860-3

  • Online ISBN: 978-1-4757-5858-0

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