The cellular mechanisms of learning in Aplysia: Of blind men and elephants

Biological Bulletin

Volumn 210, Issue 3, 2006, Pages 271-279

  Glanzman, David L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE RECEPTOR;

BRAIN; MEMORY; NEUROLOGY; SNAIL; SUBSTRATE;

ANIMAL; APLYSIA; BIOLOGICAL MODEL; CYTOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; HABITUATION; LEARNING; METABOLISM; NERVE CELL PLASTICITY; PHYSIOLOGY; REVIEW; SENSORY NERVE CELL; SYNAPSE;

ANIMALS; APLYSIA; EXCITATORY POSTSYNAPTIC POTENTIALS; HABITUATION, PSYCHOPHYSIOLOGIC; LEARNING; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEURONS, AFFERENT; RECEPTORS, GLUTAMATE; SYNAPSES;

APLYSIA; ELEPHANTIDAE; GASTROPODA; MAMMALIA;

EID: 33745714918     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/4134563     Document Type: Review

References (85)

1. Antonov, I., I. Antonova, E. R. Kandel, and R. D. Hawkins. 2003. Activity-dependent presynaptic facilitation and Hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37: 135-147.
2. Antonova, I., O. Arancio, A.-C. Trillat, H.-G. Wang, L. Zablow, H. Udo, E. R. Kandel, and R. D. Hawkins. 2001. Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation. Science 294: 1547-1550.
3. Antzoulatos, E. G., L. J. Cleary, A. Eskin, D. A. Baxter, and J. H. Byrne. 2003. Desensitization of postsynaptic glutamate receptors contributes to high-frequency homosynaptic depression of Aplysia sensorimotor connections. Learn. Mem. 10: 309-313.
4. Armitage, B. A., and S. A. Siegelbaum. 1998. Presynaptic induction and expression of homosynaptic depression at Aplysia sensorimotor neuron synapses. J. Neurosci. 18: 8770-8779.
5. Bailey, C. H., and M. Chen. 1983. Morphological basis of long-term habituation and sensitization in Aplysia. Science 220: 91-93.
6. Bailey, C. H., and M. Chen. 1988a. Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. Proc. Natl. Acad. Sci. USA 85: 2373-2377.
7. Bailey, C. H., and M. Chen. 1988b. Morphological basis of short-term habituation in Aplysia. J. Neurosci. 8: 2452-2459.
8. Bao, J. X., E. R. Kandel, and R. D. Hawkins. 1998. Involvement of presynaptic and postsynaptic mechanisms in a cellular analog of classical conditioning at Aplysia sensory-motor neuron synapses in isolated cell culture. J. Neurosci. 18: 458-466.
9. Bear, M. F., B. W. Connors, and M. A. Paradiso. 2007. Neuroscience: Exploring the Brain, 3rd ed. Lippincott, Williams & Wilkins, Baltimore, MD.
10. Brunelli, M., V. Castellucci, and E. R. Kandel. 1976. Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science 194: 1178-1181.
11. Burrell, B. D., and C. L. Sahley. 2004. Multiple forms of long-term potentiation and long-term depression converge on a single interneuron in the leech CNS. J. Neurosci. 24: 4011-4019.
12. Byrne, J. H. 1987. Cellular analysis of associative learning. Physiol. Rev. 67: 329-439.
13. Byrne, J. H., and E. R. Kandel. 1996. Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 16: 425-435.
14. Cai, D., Q. Li, and D. L. Glanzman. 2005. Serotonin-induced long-term hyperexcitability of Aplysia sensory neurons in culture: dependence upon a retrograde signal from the postsynaptic motor neuron. Soc. Neurosci. Abstr. 31: 540.51. [Online].
15. Carew, T. J., and E. R. Kandel. 1973. Acquisition and retention of long-term habituation in Aplysia: correlation of behavioral and cellular processes. Science 182: 1158-1160.
16. Carew, T. J., H. M. Pinsker, and E. R. Kandel. 1972. Long-term habituation of a defensive withdrawal reflex in Aplysia. Science 175: 451-454.
17. Carew, T. J., R. D. Hawkins, T. W. Abrams, and E. R. Kandel. 1984. A test of Hebb's postulate at identified synapses which mediate classical conditioning in Aplysia. J. Neurosci. 4: 1217-1224.
18. Castellucci, V. F., and E. R. Kandel. 1974. A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. Proc. Natl. Acad. Sci. USA 71: 5004-5008.
19. Castellucci, V., H. Pinsker, I. Kupfermann, and E. R. Kandel. 1970. Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167: 1745-1748.
20. Chin, J., J. A. Burdohan, A. Eskin, and J. H. Byrne. 2002. Inhibitor of glutamate transport alters synaptic transmission at sensorimotor synapses in Aplysia. J. Neurophysiol. 87: 3165-3168.
21. Chitwood, R. A., Q. Li, and D. L. Glanzman. 2001. Serotonin facilitates AMPA-type responses in isolated siphon motor neurons of Aplysia in culture. J. Physiol. 534: 501-510.
22. Choi, S., J. Klingauf, and R. W. Tsien. 2003. Fusion pore modulation as a presynaptic mechanism contributing to expression of long-term potentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 695-705.
23. Cleary, L. J., J. H. Byrne, and W. N. Frost. 1995. Role of interneurons in defensive withdrawal reflexes in Aplysia. Learn. Mem. 2: 133-151.
24. Cohen, T. E., S. W. Kaplan, E. R. Kandel, and R. D. Hawkins. 1997. A simplified preparation for relating cellular events to behavior: mechanisms contributing to habituation, dishabituation, and sensitization of the Aplysia gill-withdrawal reflex. J. Neurosci. 17: 2886-2899.
25. Contractor, A., C. Rogers, C. Maron, M. Henkemeyer, G. T. Swanson, and S. F. Heinemann. 2002. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296: 1864-1869.
26. Dale, N., and E. R. Kandel. 1993. L-glutamate may be the fast excitatory transmitter of Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA 90: 7163-7167.
27. Dale, N., E. R. Kandel, and S. Schacher. 1987. Serotonin produces long-term changes in the excitability of Aplysia sensory neurons in culture that depend on new protein synthesis. J. Neurosci. 7: 2232-2238.
28. Dudek, S. M., and M. F. Bear. 1992. Homosynaptic long-term depression in area CA1 of the hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl. Acad. Sci. USA 89: 4363-4367.
29. Ezzeddine, Y., and D. L. Glanzman. 2003. Prolonged habituation of the gill-withdrawal reflex in Aplysia depends on protein synthesis, protein phosphatase activity, and postsynaptic glutamate receptors. J. Neurosci. 23: 9585-9594.
30. Ezzeddine, Y., K. C. Pearce, and D. L. Glanzman. 2004. Long-term habituation of the gill-withdrawal reflex in Aplysia depends upon RNA synthesis and phosphatase 2B activity. Soc. Neurosci. Abstr. 30: 553.13. [Online].
31. Frost, L., S. W. Kaplan, T. E. Cohen, V. Henzi, E. R. Kandel, and R. D. Hawkins. 1997. A simplified preparation for relating cellular events to behavior: contribution of LE and unidentified siphon sensory neurons to mediation and habituation of the Aplysia gill- and siphon-withdrawal reflex. J. Neurosci. 17: 2900-2913.
32. Frost, W. N., and E. R. Kandel. 1995. Structure of the network mediating siphon-elicited siphon withdrawal in Aplysia. J. Neurophysiol. 73: 2413-2427.
33. Glanzman, D. L. 1994. Postsynaptic regulation of the development and long-term plasticity of Aplysia sensorimotor synapses in cell culture. J. Neurobiol. 25: 666-693.
34. Glanzman, D. L., S. L. Mackey, R. D. Hawkins, A. M. Dyke, P. E. Lloyd, and E. R. Kandel. 1989. Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock. J. Neurosci. 9: 4200-4213.
35. Glanzman, D. L., E. R. Kandel, and S. Schacher. 1990. Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249: 799-802.
36. Hawkins, R. D., and E. R. Kandel. 1984. Is there a cell biological alphabet for simple forms of learning? Psychol. Rev. 91: 375-391.
37. Hawkins, R. D., T. W. Abrams, T. J. Carew, and E. R. Kandel. 1983. A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science 219: 400-405.
38. Hawkins, R. D., T. E. Cohen, W. Greene, and E. R. Kandel. 1998. Relationships between dishabituation, sensitization, and inhibition of the gill- and siphon-withdrawal reflex in Aplysia californica: effects of response measure, test time, and training stimulus. Behav. Neurosci. 112: 24-38.
39. Hochner, B., M. Klein, S. Schacher, and E. R. Kandel. 1986. Additional component in the cellular mechanism of presynaptic facilitation contributes to behavioral dishabituation in Aplysia, Proc. Natl. Acad. Sci. USA 83: 8794-8798.
40. Huang, Y.-Y., X.-C. Li, and E. R. Kandel. 1994. cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79: 69-79.
41. Kandel, E. R. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294: 1030-1038.
42. Kandel, E. R., M. Brunelli, J. Byrne, and V. Castellucci. 1975. A common presynaptic locus for the synaptic changes underlying short-term habituation and sensitization of the gill-withdrawal reflex in Aplysia. Cold Spring Harbor Symp. Quant. Biol. 40: 465-482.
43. Kirkwood, A., and M. F. Bear. 1994. Homosynaptic long-term depression in the visual cortex. J. Neurosci. 14: 3404-3412.
44. Levenson, J., D. M. Sherry, L. Dryer, J. Chin, J. H. Byrne, and A. Eskin. 2000. Localization of glutamate and glutamate transporters in the sensory neurons of Aplysia. J. Comp. Neurol. 423: 121-131.
45. 2+ from postsynaptic intracellular stores, postsynaptic exocytosis and modulation of postsynaptic AMPA receptor efficacy. J. Neurosci. 25: 5623-5637.
46. Liao, X., C. G. Brou, and E. T. Walters. 1999. Limited contributions of serotonin to long-term hyperexcitability of Aplysia sensory neurons. J. Neurophysiol. 82: 3223-3235.
47. Lin, X. Y., and D. L. Glanzman. 1994a. Hebbian induction of long-term potentiation of Aplysia sensorimotor synapses: partial requirement for activation of an NMDA-related receptor. Proc. Biol. Sci. 255: 215-221.
48. Lin, X. Y., and D. L. Glanzman. 1994b. Long-term potentiation of Aplysia sensorimotor synapses in cell culture: regulation by postsynaptic voltage. Proc. Biol. Sci. 255: 113-118.
49. Lin, X. Y., and D. L. Glanzman. 1996. Long-term depression of Aplysia sensorimotor synapses in cell culture: inductive role of a rise in postsynaptic calcium. J. Neurophysiol. 76: 2111-2114.
50. Lisman, J., H. Schulman, and H. Cline. 2002. The molecular basis of CaMKII function in synaptic and behavioral memory. Nat. Rev. Neurosci. 3: 175-190.
51. Lledo, P. M., X. Zhang, T. C. Seudhof, R. C. Malenka, and R. A. Nicoll. 1998. Postsynaptic membrane fusion and long-term potentiation. Science 279: 399-403.
52. Mackey, S. L., E. R. Kandel, and R. D. Hawkins. 1989. Identified serotonergic neurons LCB1 and RCB1 in the cerebral ganglia of Aplysia produce presynaptic facilitation of siphon sensory neurons. J. Neurosci. 9: 4227-4235.
53. Malinow, R., and R. C. Malenka. 2002. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25: 103-126.
54. Malenka, R. C., and M. F. Bear. 2004. LTP and LTD: an embarrassment of riches. Neuron 44: 5-21.
55. Malenka, R. C., and R. A. Nicoll. 1999. Long-term potentiation - a decade of progress? Science 285: 1870-1874.
56. Marcus, E. A., T. G. Nolen, C. H. Rankin, and T. J. Carew. 1988. Behavioral dissociation of dishabituation, sensitization, and inhibition in Aplysia. Science 241: 210-213.
57. Marinesco, S., and T. J. Carew. 2002. Serotonin release evoked by tail nerve stimulation in the CNS of Aplysia: characterization and relationship to heterosynaptic plasticity. J. Neurosci. 22: 2299-2312.
58. Mellor, J., and R. A. Nicoll. 2001. Hippocampal mossy fiber LTP is independent of postsynaptic calcium. Nat. Neurosci. 4: 125-126.
59. Montarolo, P. G., P. Goelet, V. F. Castellucci, J. Morgan, E. R. Kandel, and S. Schacher. 1986. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234: 1249-1254.
60. Morris, R. G., E. I. Moser, G. Riedel, S. J. Martin, J. Sandin, M. Day, and C. O'Carroll. 2003. Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 773-786.
61. Mulkey, R. M., and R. C. Malenka. 1992. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9: 967-975.
62. Mulkey, R. M., C. E. Herron, and R. C. Malenka. 1993. An essential role for protein phosphatases in hippocampal long-term depression. Science 261: 1051-1055.
63. Mulkey, R. M., S. Endo, S. Shenolikar, and R. C. Malenka. 1994. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369: 486-488.
64. 2+. Proc. Natl. Acad. Sci. USA 93: 9931-9936.
65. Murphy, G. G., and D. L. Glanzman. 1997. Mediation of classical conditioning in Aplysia californica by LTP of sensorimotor synapses. Science 278: 467-471.
66. Murphy, G. G., and D. L. Glanzman. 1999. Cellular analog of differential classical conditioning in Aplysia: disruption by the NMDA receptor-antagonist DL-2-amino-5-phosphonovalerate. J. Neurosci. 19: 10595-10602.
67. Nicoll, R. A. 2003. Expression mechanisms underlying long-term potentiation: a postsynaptic view. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 721-726.
68. Pinsker, H., I. Kupfermann, V. Castellucci, and E. Kandel. 1970. Habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167: 1740-1742.
69. Powell, C. M. 2006. Gene targeting of presynaptic proteins in synaptic plasticity and memory: across the great divide. Neurobiol. Learn. Mem. 85: 2-15.
70. Rankin, C. H., and T. J. Carew. 1988. Dishabituation and sensitization emerge as separate processes during development in Aplysia. J. Neurosci. 8: 197-211.
71. Rankin, C. H., and S. R. Wicks. 2000. Mutations of the Caenorhabditis elegans brain-specific inorganic phosphate transporter eat-4 affect habituation of the tap-withdrawal response without affecting the response itself. J. Neurosci. 20: 4337-4344.
72. Roberts, A. C., and D. L. Glanzman. 2003. Learning in Aplysia: looking at synaptic plasticity from both sides. Trends Neurosci. 26: 662-670.
73. Rose, J. K., and C. H. Rankin. 2001. Analyses of habituation in Caenorhabditis elegans. Learn. Mem. 8: 63-69.
74. Rose, J. K., K. R. Kaun, S. H. Chen, and C. H. Rankin. 2003. GLR-1, a non-NMDA glutamate receptor homolog, is critical for long-term memory in Caenorhabditis elegans. J. Neurosci. 23: 9595-9599.
75. Rumpel, S., J. LeDoux, A. Zador, and R. Malinow. 2005. Postsynaptic receptor trafficking underlying a form of associative learning. Science 308: 83-88.
76. Trudeau, L. E., and V. F. Castellucci. 1993a. Excitatory amino acid neurotransmission at sensory-motor and interneuronal synapses of Aplysia californica. J. Neurophysiol. 70: 1221-1230.
77. Trudeau, L. E., and V. F. Castellucci. 1993b. Functional uncoupling of inhibitory interneurons plays an important role in short-term sensitization of Aplysia gill and siphon withdrawal reflex. J. Neurosci. 13: 2126-2135.
78. Tsau, Y., J. Y. Wu, H. P. Hopp, L. B. Cohen, D. Schiminovich, and C. X. Falk. 1994. Distributed aspects of the response to siphon touch in Aplysia: spread of stimulus information and cross-correlation analysis. J. Neurosci. 14: 4167-4184.
79. Walters, E. T., and J. H. Byrne. 1983. Associative conditioning of single sensory neurons suggests a cellular mechanism for learning. Science 219: 405-408.
80. Weisskopf, M. G., P. E. Castillo, R. A. Zalutsky, and R. A. Nicoll. 1994. Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265: 1878-1882.
81. Williams, S., and D. Johnston. 1989. Long-term potentiation of hippocampal mossy fiber synapses is blocked by postsynaptic injection of calcium chelators. Neuron 3: 583-588.
82. Xia, S., T. Miyashita, T. F. Fu, W. Y. Lin, C. L. Wu, L. Pyzocha, I. R. Lin, M. Saitoe, T. Tully, and A. S. Chiang. 2005. NMDA receptors mediate olfactory learning and memory in Drosophila. Curr. Biol. 15: 603-615.
83. Yeckel, M. F., A. Kapur, and D. Johnston. 1999. Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nat. Neurosci. 2: 625-633.
84. Zakharenko, S. S., S. L. Patterson, I. Dragatsis, S. O. Zeitlin, S. A. Siegelbaum, E. R. Kandel, and A. Morozov. 2003. Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39: 975-990.
85. Zalutsky, R. A., and R. A. Nicoll. 1990. Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248: 1619-1624.