Cellular Mechanisms of Classical Conditioning

  • Bernard G. Schreurs
  • Daniel L. Alkon


The search for the cellular mechanisms of learning and memory has fostered the development of a large number of model systems, preparations that demonstrate learning and are tractable to biological analyses. We examine briefly the history and status of classical conditioning as a means of studying the biological basis of associative learning. Several model systems, including Aplysia, Hermissenda, Drosophila, and the rabbit nictitating membrane response, are examined for their ability to demonstrate associative learning when classical conditioning procedures are employed. The cellular mechanisms of learning and memory are assessed in light of the types of behavior change that these model systems exhibit.


Purkinje Cell Unconditioned Stimulus Classical Conditioning Associative Learning Unconditioned Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abel, T., and Kandel, E. (1998). Positive and negative regulatory mechanisms that mediate long-term memory storage. Brain Research Reviews, 26, 360–378.PubMedGoogle Scholar
  2. Aleksandrov, A.V., Vasil’eva, O.N., Ioffe, M.E., and Frolov, A.A. (1992). Certain methods of biomechanical description of various postural adjustment patterns during motoric learning in dogs. Neuroscience and Behavioral Physiology, 22, 503–512.PubMedGoogle Scholar
  3. Alkon, D.L. (1983). Learning in marine snails. Scientific American, 249, 70–84.PubMedGoogle Scholar
  4. Alkon, D.L. (1987). Memory traces in the brain. New York: Cambridge University Press.Google Scholar
  5. Alkon, D.L. (1989). Memory storage and neural systems. Scientific American, 261, 42–50.PubMedGoogle Scholar
  6. Alkon, D.L., Nelson, T.J., Zhao, W., and Cavallaro, S, (1998). Time domains of neuronal Ca2+ signaling and associative memory: steps through a calexcitin, ryanodine receptor, K+ channel cascade. Trends in Neuroscience, 21, 529–537.Google Scholar
  7. Allen, A., Michels, J., and Young, J.Z. (1985). Memory and visual discrimination by squids. Marine Behavior and Physiology, 11, 271–282.Google Scholar
  8. Ayers, J.J.B., Benedict, J.O., and Wichter, E.S. (1975). Systematic manipulation of individual events in a truly random control in rats. Journal of Comparative and Physiological Psychology, 88, 97–103.Google Scholar
  9. Baily, C.H., and Kandel, E.R. (1993). Structural changes accompanying membrane storage. Annual Review of Physiology, 55, 397–426.Google Scholar
  10. Bao, J.X., Kandel, E.R., and Hawkins, R.D. (1998). Involvement of presynaptic and postsynaptic mechanisms in a cellular analog of classical conditioning at Aplysia sensorymotor neuron synapses in isolated cell culture. Journal of Neuroscience, 18, 458–466.PubMedGoogle Scholar
  11. Benedict, J.O., and Ayers, J.J.B. (1972). Factors affecting conditioning in the truly random control procedure in the rat. Journal of Comparative and Physiological Psychology, 78, 323–330.PubMedGoogle Scholar
  12. Biegler, R., and Morris, R.G. (1993). Landmark stability is a prerequisite for spatial but not discrimination learning. Nature, 361, 631–663.PubMedGoogle Scholar
  13. Bliss, T.V.P., and Collingridge, G.L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 261, 31–39.Google Scholar
  14. Bliss, T.V.P., and Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. Journal of Physiology (London), 232, 331–356.Google Scholar
  15. Boakes, R.A. (1977). Performance on learning to associate a stimulus with positive reinforcement. In H. Davis and H.M.B. Hurwitz (Eds.), Operant Pavlovian interactions (pp. 67–97). Hillsdale, NJ: Erlbaum.Google Scholar
  16. Brigui, N., Le Bourg, E., and Medioni, J. (1990). old Drosophila melanogaster flies: acquisition and extinction. Journal of Comparative Psychology, 104, 289–296.PubMedGoogle Scholar
  17. Brown, G.D. (1998). Operational terminology for stimulus exposure (SE) conditioning. Behavioural Brain Research, 95, 143–150.PubMedGoogle Scholar
  18. Buonomano, D.V., and Merzenich, M.M. (1998). Cortical plasticity: from synapses to maps. Annual Review of Neuroscience, 21, 149–186.PubMedGoogle Scholar
  19. Carew, T.J., Hawkins, R.D., and Kandel, E.R. (1983). Differential classical conditioning of a defensive withdrawal reflex in Aplysia. Science, 219, 397–400.PubMedGoogle Scholar
  20. Carew, T.J., Walters, E.T., and Kandel, E.R. (1981). Classical conditioning in a simple withdrawal reflex in Aplysia californica. Journal of Neuroscience, 1, 1426–1437.PubMedGoogle Scholar
  21. Cohen, D.H. (1980). The functional neuroanatomy of a conditioned response. In R.F. Thompson, L.H. Hicks, and V.B. Shvyrkov (Eds.), Neural mechanisms of goal-directed behavior and learning (pp. 283–302). New York: Academic Press.Google Scholar
  22. De Jianne, D., McGuire, T.R., and Pruzan-Hotchkiss, A. (1985). Conditioned suppression of proboscis extension in Drosophila melanogaster. Journal of Comparative Psychology, 99, 74–80.Google Scholar
  23. Dubnau, J., and Tully, T. (1998). Gene discovery in Drosophila: new insights for learning and memory. Annual Review of Neuroscience, 21, 407–444.PubMedGoogle Scholar
  24. Ebbinghaus, H. (1885). Uber das gedachtnis. Leipzig: Duncker and Humbolt. [Translated by H.A. Ruger and Clara Bussenins (1913) in Memory. New York: Columbia.]Google Scholar
  25. Etcheberrigaray, R., Ito, E., Kim, C.S., and Alkon, D.L. (1994a). Soluble β-amyloid induction of Alzheimer’s phenotype for human fibroblast K+ channels. Science, 264, 276–279.PubMedGoogle Scholar
  26. Etcheberrigaray, R., Gibson, G.E., and Alkon, D.L. (1994b). Molecular mechanisms of memory and the pathophysiology of Alzheimer’s disease. Annals of the New York Academy of Sciences, 747, 245–255.PubMedGoogle Scholar
  27. Etcheberrigaray, R., Payne, J.L., and Alkon, D.L. (1996). Soluble beta-amyloid induces Alzheimer’s disease features in human fibroblasts and in neuronal tissues. Life Sciences, 59, 491–498.PubMedGoogle Scholar
  28. Freeman, J.H., Jr., Scharenberg, A.M., Olds, J.L., and Schreurs, B.G. (1998). Classical conditioning increases membrane-bound protein kinase C in rabbit cerebellum. Neuro Report, 9, 2669–2673.Google Scholar
  29. Fresquet, N., and Medioni, J. (1993). Effects of aging on visual discrimination learning in Drosphila melanogaster. Quarterly Journal of Experimental Psychology, 46, 399–412.PubMedGoogle Scholar
  30. Gelperin, A. (1994). Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc. Nature, 369, 61–63.PubMedGoogle Scholar
  31. Glanzman, D.L. (1995). The cellular basis of classical conditioning in Aplysia californica—it’s not as simple as you think. Trends in Neuroscience, 18, 30–36.Google Scholar
  32. Goodwin, S.F., Del Vecchio, M., Velinzon, K., Hogel, C. Russell, S.R.H., Tully, T., and Kaiser, T. (1997). Defective learning in mutants of the Drosophila gene for regulatory subunit of cAMP-dependent protein kinase. Journal of Neuroscience, 17, 8817–8827.PubMedGoogle Scholar
  33. Gormezano, I. (1966). Classical conditioning. In J.B. Sidowski (Ed.), Experimental methods and instrumentation in psychology (pp. 385–420). New York: McGraw-Hill.Google Scholar
  34. Gormezano, I., and Kehoe, E.J. (1975) Classical conditioning: some methodological-conceptual issues. In W.K. Estes, (Ed.), Handbook of learning and cognitive processes, Vol. 2. Conditioning and behavior theory (pp. 143–179). Hillsdale, NJ: Erlbaum.Google Scholar
  35. Gormezano, I., and Kehoe, E.J. (1981). Classical conditioning and the law of contiguity. In P. Harzern and M.D. Zeiler (Eds.), Advances in analysis of behavior. Vol. 2. Predictability, correlation, and contiguity (pp. 1–45). Sussex, England: Wiley & Sons.Google Scholar
  36. Gormezano, I., and Tait, R.W. (1976). The Pavlovian analysis of instrumental conditioning. Pavlovian Journal of Biological Sciences, 11, 37–55.Google Scholar
  37. Gormezano, I., Kehoe, E.J., and Marshall, B. (1983). Twenty years of classical conditioning research with the rabbit. In J.M. Sprague and A.N. Epstein (Eds.), Progress in psychobiology and physiological psychology, Vol. 11. (pp. 197–275). New York: Academic Press.Google Scholar
  38. Gormezano, I., Schneiderman, N., Deaux, E.G., and Fuentes, I. (1962). Nictitating membrane: classical conditioning and extinction in the albino rabbit. Science, 138, 33–34.PubMedGoogle Scholar
  39. Grant, D.A. (1943). Sensitization and association in eyelid conditioning. Journal of Experimental Psychology, 32, 201–212.Google Scholar
  40. Grant, D.A. (1944). A sensitized eyelid reaction related to the conditioned eyelid response. Journal of Experimental Psychology, 35, 393–404.Google Scholar
  41. Grant, D.A., and Adams, J.K. (1944). ‘Alpha’ conditioning in the eyelid. Journal of Experimental Psychology, 34, 136–142.Google Scholar
  42. Gruart, A., Blazquez, P., and Delgado-Garcia, J.M. (1995). Kinematics of spontaneous, reflex and conditioned eyelid movements in the alert cat. Journal of Neurophysiology, 74, 226–248.PubMedGoogle Scholar
  43. Harris, C.L. (1991). An improved Horridge procedure for studying leg-position learning in cockroaches. Physiology & behavior, 49, 543–548.Google Scholar
  44. Hawkins, R.D., and Kandel, E.R. (1984). Is there a cell-biological alphabet for simple forms of learning? Psychological Review, 91, 375–391.PubMedGoogle Scholar
  45. Hawkins, R.D., Carew, T.J., and Kandel, E.R. (1986). Effects of interstimulus interval and contingency on classical conditioning of Aplysia siphon-withdrawal reflex. Journal of Neuroscience, 6, 1695–1701.PubMedGoogle Scholar
  46. Hawkins, R.D., Greene, W., and Kandel, E.R. (1998a). second-order conditioning of the Aplysia gill-withdrawal reflex in a simplified mantle organ preparation. Behavioral Neuroscience, 112, 636–645.PubMedGoogle Scholar
  47. Hawkins, R.D., Cohen, T.E., Greene, W., and Kandel, E.R. (1998b). inhibition of the gill-and siphon-withdrawal reflex in Aplysia californica: effects of response measure, test time, and training stimulus. Behavioral Neuroscience, 112, 24–38.PubMedGoogle Scholar
  48. Hearst, E., and Jenkins, H.M. (1974). Sign tracking: the stimulus reinforcer relation and directed action. Monograph. Austin, TX: Psychonomic Society.Google Scholar
  49. Hirsch, J., and Holliday, M. (1988). A fundamental distinction in the analysis and interpretation of behavior. Journal of Comparative Psychology, 102, 372–377.PubMedGoogle Scholar
  50. Holland, P.C. (1980). Influence of visual conditioned stimulus characteristics on the form of Pavlovian appetitive conditioned responding in rats. Journal of Experimental Psychology: Animal Behavior Processes, 6, 81–97.PubMedGoogle Scholar
  51. Holliday, M. and Hirsch, J. (1986). Excitatory conditioning of individual Drosophila melanogaster. Journal of Experimental Psychology: Animal Behavior Processes, 12, 131–142.PubMedGoogle Scholar
  52. Jenkins, H.M., and Moore, B.R. (1973). The form of the autoshaped response with food or water reinforcers. Journal of the Experimental Analysis of behavior, 20, 163–181.PubMedGoogle Scholar
  53. Kandel, E.R. (1976) Cellular basis of behavior: an introduction to behavioral neurobiology. San Francisco, Free Press.Google Scholar
  54. Keifer, J., Armstrong, K.E., and Houk, J.C. (1995). In vitro classical conditioning of abducens nerve discharge in turtles. Journal of Neuroscience, 15, 5036–5048.PubMedGoogle Scholar
  55. Kim, E.H.-J., Woody, CD., and Berthier, N.E. (1983). Rapid acquisition of conditioned eye-blink responses in cats following pairing of an auditory CS with a glabellar-tap US and hypothalamic stimulation. Journal of Neurophysiology, 49, 161–119.Google Scholar
  56. Krasne, F.B., and Teshiba, T. (1995). Habituation of an invertebrate escape reflex due to modulation by higher centers rather than local events. Proceedings of the National Academy of Sciences of the United States of America, 92, 3362–3366.PubMedGoogle Scholar
  57. Krupa, D.J., Weng, J., and Thompson, R.F. (1996). Inactivation of brainstem nuclei blocks expression but not acquisition of the rabbit’s classically conditioned eyeblink response. Behavioral Neuroscience, 110, 219–227.PubMedGoogle Scholar
  58. Kulitka, E.F. (1992). Influence of superficial polarization of the cerebral cortex of the dog on extinctive inhibition. Neuroscience & Behavioral Physiology, 22, 56–58.Google Scholar
  59. Lederhendler, I., Gart, S., and Alkon, D.L. (1986). Classical conditioning of Hermissenda: origin of a new response. Journal of Neuroscience, 6, 1325–1331.PubMedGoogle Scholar
  60. Leonard, J.L., Edstrom, J., and Lukowiak, K. (1989). Reexamination of the gill withdrawal reflex of Aplysia californica Cooper (Gastropoda: Opisthobranchia). Behavioral Neuroscience, 103, 585–604.PubMedGoogle Scholar
  61. Linden, D.J., and Connor, J.A. (1995). Long-term depression. Annual Review of Neuroscience, 18, 319–357.PubMedGoogle Scholar
  62. Lofdahl, K.L., Holliday, M.J., and Hirsch, J. (1992). Selection for conditionability in Drosophila melanogster. Journal of Comparative Psychology, 106, 172–183.PubMedGoogle Scholar
  63. Mackintosh, N.J. (1983). Conditioning and associative learning. Oxford: Oxford University Press.Google Scholar
  64. Matzel, L.D., Schreurs, B.G., and Alkon, D.L. (1990a). Pavlovian conditioning of distinct components of Hermissenda’s response to rotation. Behavioral and Neural Biology, 54, 131–145.PubMedGoogle Scholar
  65. Matzel, L.D., Schreurs, B.G., Lederhendler, I., and Alkon, D.L. (1990b). Acquisition of conditioned associations in Hermissenda: additive effects of contiguity and the forward interstimulus interval. Behavioral Neuroscience, 104, 597–606.PubMedGoogle Scholar
  66. Medioni, J., and Vaysse, G. (1975). Suppression conditionnelle d’un reflexe chez la Drosphile Drosophila melanogaster): acquistion et extinction. Comptes Rendus des Seances de la Societe de Biologie, 169, 1386–1391.Google Scholar
  67. Mein, N., Ghelardini, C., Tesco, G., Galeotti, N., Dahl, D., Tomsic, D., Cavallaro, S., Quattrone, A., Capaccioli, S., Bartolini, A., and Alkon, D.L. (1997). Reversible antisense inhibition of shaker-like Kv1.1 potassium channel expression impairs associative memory in mouse and rat. Proceedings of the National Academy of Sciences of the United States of America, 94, 4430–4434.Google Scholar
  68. Menzel, R., and Muller, R. (1996). Learning and memory in honeybees: from behavior to neural substrates. Annual Review of Neuroscience, 19, 379–404.PubMedGoogle Scholar
  69. Michels, J., Robertson, J.D., and Young, J.Z. (1987). Can conditioned aversive tactile stimuli affect extinction of visual responses in octopus? Marine Behavior & Physiology, 13, 1–11.Google Scholar
  70. Milner, B., Squire, L.R., and Kandel, E.R. (1998). Cognitive neuroscience and the study of memory. Neuron, 20, 445–468.PubMedGoogle Scholar
  71. Minois, N., and Le Bourg, E. (1997). Hypergravity and aging in Drosophila melanogaster. 9. Conditioned suppression and habituation of the proboscis extension response. Aging Clinical and Experimental Research, 9, 281–291.Google Scholar
  72. Mishkin, M. (1982). A memory system in the monkey. Philosophical Transactions of the Royal Society of London, 298, 85–95.Google Scholar
  73. Molchan, S.E., Sunderland, T., Mclntosh, A.R., Herscovitch, P., and Schreurs, B.G. (1994). A functional anatomical study of associative learning in humans. Proceedings of the National Academy of Sciences of the United States of America, 91, 8122–8126.PubMedGoogle Scholar
  74. Nelson, T.J., Zhao, W.Q., Yuan, S., Favit, A., Pozzo-Miller, L., and Alkon, D.L. (1999). Calexcitin interaction with neuronal ryanodine receptors. Biochemical Journal, 341, 423–433.PubMedGoogle Scholar
  75. Olds, J.L., Anderson, M., McPhie, D., Staten, L., and Alkon, D.L. (1989). Imaging memory-specific changes in the distribution of protein kinase C within the hippocampus. Science, 245, 866–869.PubMedGoogle Scholar
  76. Pavlov, I.P. (1927). Conditioned reflexes. (Translated by G.V. Anrep.) London: Oxford University Press.Google Scholar
  77. Preat, T. (1998). Decreased odor avoidance after electrical shock in Drosophila mutants biases learning and memory tests. Journal of Neuroscience, 18, 8534–8538.PubMedGoogle Scholar
  78. Rescorla, R.A. (1988). Pavlovian conditioning. It’s not what you think. American Psychologist, 43, 151–160.PubMedGoogle Scholar
  79. Ricker, J.P., Hirsch, J., Holliday, M., and Vargo, M.A. (1986). An examination of claims for classical conditioning as a phenotype in the genetic analysis of Diptera. In J.L. Fuller and E.C. Simmel (Eds.), Perspectives in behavior genetics (pp. 155–200). Hillsdale, NJ: Erlbaum.Google Scholar
  80. Sahley, C.L. (1994). Serotonin depletion impairs but does not eliminate classical conditioning in the leech Hirudo medicinalis. Behavioral Neuroscience, 108, 1043–1052.PubMedGoogle Scholar
  81. Sanchez-Andres, J.V., and Alkon, D.L. (1991). Voltage-clamp analysis of the effects of classical conditioning on the hippocampus. Journal of Neurophysiology, 65, 796–807.PubMedGoogle Scholar
  82. Schneiderman, N., McCabe, P.M., Haselton, J.R., Ellenberger, H.H., Jarrell, T.W., and Gentile, C.G. (1987). Neurobiological bases of conditioned bradycardia in rabbits. In I. Gormezano, W.F. Prokasy, and R.F. Thompson (Eds.), Classical conditioning (3rd ed.) (pp. 37–63). Hillsdale, NJ: Erlbaum.Google Scholar
  83. Schreurs, B.G. (1989). Classical conditioning of model systems: a behavioral review. Psychobiology 17, 145–155.Google Scholar
  84. Schreurs, B.G., and Alkon, D.L. (1990). US-US conditioning of the rabbit’s nictitating membrane response: emergence of a conditioned response without alpha conditioning. Psychobiology 18, 312–320.Google Scholar
  85. Schreurs, B.G., and Alkon, D.L. (1993). Rabbit cerebellar slice analysis of long-term depression and its role in classical conditioning. Brain Research, 631, 235–240.PubMedGoogle Scholar
  86. Schreurs, B.G., Sanchez-Andres, J.V., and Alkon, D.L. (1991). Learning-specific differences in Purkinje-cell dendrites of lobule HVI (lobulus simplex): intracellular recording in a rabbit cerebellar slice. Brain Research, 548, 18–22.PubMedGoogle Scholar
  87. Schreurs, B.G., Tomsic, D., Gusev, P.A., and Alkon, D.L. (1997a). Dendritic excitability microzones and occluded long-term depression after classical conditioning of the rabbit’s nictitating membrane response. Journal of Neurophysiology, 77, 86–92.PubMedGoogle Scholar
  88. Schreurs, B.G., Mclntosh, A.R., Bahro, M., Herscovitch, P, Sunderland, T., and Molchan, S.E. (1997b). Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. Journal of Neurophysiology, 77, 2153–2163.PubMedGoogle Scholar
  89. Schreurs, B.G., Gusev, P.A., Tomsic, D., Alkon, D.L., and Shi, T. (1998). Intracellular correlates of acquisition and long-term memory of classical conditioning in Purkinje cell dendrites in slices of rabbit cerebellar lobule HVI. Journal of Neuroscience, 18, 5498–5507.PubMedGoogle Scholar
  90. Skelton, R.W. (1988). Bilateral cerebellar lesions disrupt conditioned eyelid responses in unrestrained rats. Behavioral Neuroscience, 102, 586–590.PubMedGoogle Scholar
  91. Solomon, P.R., Pomerleau, D., Bennet, L., James, J., and Morse, D.L. (1989). Acquisition of the classically conditioned eyeblink response in humans over the life span. Psychology and Aging, 4, 34–41.PubMedGoogle Scholar
  92. Tang, Y.-P., Shimizu, E., Dube, G.R., Rampon, C., Kerchner, G.A., Zhou, M., Liu, G., and Tsien, J.Z. (1999). Genetic enhancement of learning and memory in mice. Nature, 401, 63–69.PubMedGoogle Scholar
  93. Thompson, R.F.(1986). The neurobiology of learning and memory. Science, 233, 941–941.PubMedGoogle Scholar
  94. Thompson, R.F., and Kim, J.J. (1996). Memory systems in the brain and localization of a memory. Proceedings of the National Academy of Sciences of the United States of America, 93, 13438–13444.PubMedGoogle Scholar
  95. Tully, T. (1996). Discovery of genes involved with learning and memory: an experimental synthesis of Hirschian and Benzerian perspectives. Proceedings of the National Academy of Sciences of the United States of America, 93, 13460–13467.PubMedGoogle Scholar
  96. Tully, T. (1997). Regulation of gene expression and its role in long-term memory and synaptic plasticity. Proceedings of the National Academy of Sciences of the United States of America, 94, 4239–4241.PubMedGoogle Scholar
  97. Tully, T., and Quinn, W.G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. Journal of Comparative Physiology, 157, 263–277.PubMedGoogle Scholar
  98. Van der Zee, E.A., Luiten, P.G.M., and Disterhoft, J.F. (1997). Learning-induced alterations in hippocampal PKC-immunoreactivity: a review and hypothesis of its functional significance. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 21, 531–572.PubMedGoogle Scholar
  99. Vargo, M., and Hirsch, J. (1982). Central excitation in the fruit fly (Drosophila melanogaster). Journal of Comparative and Physiological Psychology, 96, 452–459.PubMedGoogle Scholar
  100. Vaysse, G., and Medioni, J. (1976). Nouvelles experiences sur le conditionement et le pseudoconditionnement du reflexe tarsal chez la Drosophile (Drospohila melanogaster): effets de chocs electriques de faible intensite. Comptes Rendus des Seances de la Societe de Biologie, 170, 1299–1304.Google Scholar
  101. Wallace, B., and Sperlich, D. (1988). Conditioning the behavior of Drosophila melanogaster by means of electric shocks. Proceedings of the National Academy of Sciences of the United States of America, 85, 2869–2872.PubMedGoogle Scholar
  102. Woodruff-Pak, D.S. (1997). Classical conditioning. International Review of Neurobiology, 41, 341–366.PubMedGoogle Scholar
  103. Woody, C.D. (1970). Conditioned eye blink: gross potential activity at coronal-pericruciate cortex of the cat. Journal of Neurophysiology, 33, 838–850.PubMedGoogle Scholar
  104. Zamanillo, D., Sprengel, R., Hvalby, O., Jensen, V., Burnashev, N., Rozov, A., Kaiser, K.M.M., Kööster, H.J., Borchardt, T., Worley, P., Lüübke, J., Frotscher, M., Kelly, P.H., Sommer, B., Andersen, P., Seeburg, P.H., and Sakmann, B. (1999). Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science, 284, 1805–1811.PubMedGoogle Scholar
  105. Zawistkowski, S., and Hirsch, J. (1984). Conditioned discrimination in the blow fly, Phormia regina: controls and bidirectional selection. Animal Learning & behavior, 12, 402–408.Google Scholar
  106. Zucker, R.S. (1972). Crayfish escape behavior and central synapses. II. Neural circuit exciting lateral giant fiber. Journal of Neurophysiology, 35, 599–637.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Bernard G. Schreurs
  • Daniel L. Alkon

There are no affiliations available

Personalised recommendations