In Vitro Analog of Classical Conditioning of Feeding Behavior in Aplysia

Learning and Memory

Volumn 10, Issue 6, 2003, Pages 478-494

  Mozzachiodi, Riccardo ^a   Lechner, Hilde A ^a,b   Baxter, Douglas A ^a   Byrne, John H ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APLYSIA; ARTICLE; ASSOCIATION; CONDITIONING; ELECTROSTIMULATION; FEEDING BEHAVIOR; NERVE CELL PLASTICITY; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; TACTILE STIMULATION;

ANIMALS; APLYSIA; ASSOCIATION LEARNING; CONDITIONING, CLASSICAL; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; FEEDING BEHAVIOR; NEURONAL PLASTICITY; NEURONS, AFFERENT; SYNAPTIC TRANSMISSION;

EID: 0345060300     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.65303     Document Type: Article

References (97)

1. Abrams, T., Yovell, Y., Onyike, C., Cohen, J., and Jarrard, H. 1998. Analysis of sequence-dependent interaction between transient calcium and transmitter stimuli in activating adenylyl cyclase in Aplysia: Possible contribution to CS-US sequence requirement during conditioning. Learn. Mem. 4: 496-509.
2. Anderson, J.A. 1967. Patterns of response of neurons in the cerebral ganglion of Aplysia californica. Exp. Neurol. 19: 65-77.
3. Antonov, I., Antonova, I., Kandel, E.R., and Hawkins, R.D. 2001. The contribution of activity-dependent synaptic plasticity to classical conditioning in Aplysia. J. Neurosci. 21: 6413-6422.
4. Antonov, I., Antonova, I., Kandel, E.R., and Hawkins R.D. 2003. Activity-dependent presynaptic facilitation and Hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37: 135-147.
5. Balaban, P.M., Bravarenko, N.I., Maksimova, O.A., Nikitin, E., Ierusalimsky, V.N., and Zakharov, I.S. 2001. A single serotonergic modulatory cell can mediate reinforcement in the withdrawal network of the terrestrial snail. Neurobiol. Learn. Mem. 75: 30-50.
6. 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 sensory-motor neuron synapses in isolated cell culture. J. Neurosci. 18: 458-466.
7. Benjamin, P.R., Staras, K., and Kemenes, G. 2000. A system approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn. Mem. 7: 124-131.
8. Brembs, B., Lorenzetti, F.D., Reyes, F.D., Baxter, D.A., and Byrne, J.H. 2002. Operant reward learning in Aplysia: Neuronal correlates and mechanisms. Science 296: 1706-1709.
9. Buonomano, D.V. and Byrne, J.H. 1990. Long-term synaptic changes produced by a cellular analog of classical conditioning in Aplysia. Science 249: 420-423.
10. Byrne, J.H. 1987. Cellular analysis of associative learning. Physiol. Rev. 67: 329-439.
11. Byrne, J.H., 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.
12. Carew, T.J. and Sahley, C.L. 1986. Invertebrate learning and memory: From behavior to molecules. Annu. Rev. Neurosci. 9: 435-487.
13. 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.
14. Church, P.J. and Lloyd, P.E. 1994. Activity of multiple identified motor neurons recorded intracellularly during evoked feeding-like motor programs in Aplysia. J. Neurophysiol. 72: 1794-1809.
15. Colwill, R.M., Goodrum, K., and Martin, A. 1997. Pavlovian appetitive discriminative conditioning in Aplysia californica. Anim. Learn. Behav. 25: 268-276.
16. Cropper, E.C. and Weiss, K.R. 1996. Synaptic mechanisms in invertebrate pattern generation. Curr. Opin. Neurobiol. 6: 833-841.
17. Cropper, E.C., Kupfermann, I., and Weiss, K.R. 1990. Differential firing patterns of the peptide containing cholinergic motor neurons B15 and B16 during feeding behavior in Aplysia. Brain. Res. 522: 176-179.
18. Crow, T. 1988. Cellular and molecular analysis of associative learning and memory in Hermissenda. Trends Neurosci. 11: 136-147.
19. Crow, T. and Alkon, D.L. 1978. Retention of an associative behavioral change in Hermissenda. Science 201: 1239-1241.
20. Davis, W.J. and Gillette, R. 1978. Neural correlate of behavioral plasticity in command neurons of Pleurobranchaea. Science 199: 801-804.
21. Dubnau, J. and Tully, T. 2001. Functional anatomy: From molecule to memory. Curr. Biol. 11: R240-R243.
22. Elliott, C.J. and Susswein, A.J. 2002. Comparative neuroethology of feeding control in molluscs. J. Exp. Biol. 205: 877-896.
23. Evans, C.G. and Cropper, E.C. 1998. Proprioceptive input to feeding motor programs in Aplysia. J. Neurosci. 8: 8016-8031.
24. Fredman, S.M. and Jahan-Parwar, B. 1980. Processing of chemosensory and mechanosensory information in identifiable Aplysia neurons. Comp. Biochem. Physiol. A 66: 25-34.
25. Gandhi, C.C. and Matzel, L.D. 2000. Modulation of presynaptic action potential kinetics underlies synaptic facilitation of type B photoreceptors after associative conditioning in Hermissenda. J. Neurosci. 20: 2022-2035.
26. Gardner, D. 1971. Bilateral symmetry and interneuronal organization in the buccal ganglia of Aplysia. Science 173: 550-553.
27. -. 1977. Interconnections of identified multiaction interneurons in buccal ganglia of Aplysia. J. Neurophysiol. 40: 349-361.
28. Getting, P.A. 1975. Tritonia swimming: Triggering of a fixed action pattern. Brain Res. 95: 128-133.
29. Glanzman, D.L. 1995. The cellular basis of classical conditioning in Aplysia californica - It's less simple that you think. Trends Neurosci. 18: 30-36.
30. Hawkins, R.D., Abrams, T.W., Carew, T.J., and Kandel, E.R. 1983. A cellular mechanism of classical conditioning in Aplysia: Activity-dependent amplification of presynaptic facilitation. Science 219: 400-405.
31. Hawkins, R.D., Kandel, E.R., and Siegelbaum, S.A. 1993. Learning to modulate transmitter release: Themes and variations in synaptic plasticity. Annu. Rev. Neurosci. 16: 625-665.
32. Hawkins, R.D., Greene, W., and Kandel, E.R. 1998. Classical conditioning, differential conditioning, and second-order conditioning of the Aplysia gill-withdrawal reflex in a simplified mantle organ preparation. Behav. Neurosci. 112: 636-645.
33. Hurwitz, I., Goldstein, R.S., and Susswein, A.J. 1994. Compartmentalization of pattern-initiation and motor functions in the B31 and B32 neurons of the buccal ganglia of Aplysia californica. J. Neurophysiol. 71: 1514-1527.
34. Hurwitz, I., Neustadter, D., Morton, D.W., Chiel, H.J., and Susswein, A.J. 1996. Activity patterns of the B31/32 pattern initiators innervating the 12 muscle of the buccal mass during normal feeding movements in Aplysia californica. J. Neurophysiol. 75: 1309-1326.
35. Hurwitz, I., Kupfermann, I., and Susswein, A.J. 1997. Different roles of neurons B63 and B34 that are active during the protraction phase of buccal motor programs in Aplysia californica. J. Neurophysiol. 78: 1305-1319.
36. Hurwitz, I., Perrins, R., Xin, Y., Weiss, K.R., and Kupfermann, I. 1999. C-PR neuron of Aplysia has different effects on "feeding" cerebral interneurons, including myomodulin-positive CB1-12. J. Neurophysiol. 81: 521-534.
37. Hurwitz, I., Kupfermann, I., and Weiss, K.R. 2003. Fast synaptic connections from CB1s to pattern-generating neurons in Aplysia: Initiation and modification of motor programs. J. Neurophysiol. 89: 2120-2136.
38. Jahan-Parwar, B. and Fredman, S.M. 1976. Cerebral ganglion of Aplysia: Cellular organization and origin of nerves. Comp. Biochem. Physiol. A 54: 347-357.
39. Jing, J. and Weiss, K.R. 2001. Neural mechanisms of motor program switch in Aplysia. J. Neurosci. 21: 7349-7362.
40. -. 2002. Interneuronal basis of the generation of related but distinct motor programs in Aplysia: Implications for current neuronal models of vertebrate intralimb coordination. J. Neurosci. 22: 6228-6238.
41. Kabotyanski, E.A., Baxter, D.A., and Byrne, J.H. 1997. Involvement of neuron B4/5 in biasing the buccal CPG toward ingestion-like fictive feeding in Aplysia. Soc. Neurosci. Abstr. 23: 1046.
42. -. 1998. Identification and characterization of catecholaminergic neuron B65, which initiates and modifies patterned activity in the buccal ganglia of Aplysia. J. Neurophysiol. 79: 605-621.
43. Kabotyanski, E.A., Baxter, D.A., Cushman, S.J., and Byrne, J.H. 2000. Modulation of fictive feeding by dopamine and serotonin in Aplysia. J. Neurophysiol. 83: 374-392.
44. Kemenes, G., Staras, K., and Benjamin, P.R. 1997. In vitro appetitive classical conditioning of feeding response in the pond snail Lymnaea stagnalis. J. Neurophysiol. 78: 2351-2361.
45. -, 2001. Multiple types of control by identified interneurons in a sensory-activated rhythmic motor pattern. J. Neurosci. 21: 2903-2911.
46. Kemenes, I., Kemenes, G., Andrew, R.J., Benjamin, P.R., and O'Shea, M. 2002. Critical time-window for NO-cGMP-dependent long-term memory formation after one-trial appetitive conditioning. J. Neurosci. 22: 1414-1425.
47. Kirk, M.D. 1989. Premotor neurons in the feeding system of Aplysia californica. J. Neurobiol. 20: 497-512.
48. Kovac, M.P., Matera, E.M., Volk, P.J., and Davis, W.J. 1986. Food avoidance learning is accompanied by synaptic attenuation in identified interneurons controlling feeding behavior in Pleurobranchaea. J. Neurophysiol. 56: 891-905.
49. Kuslansky, B., Weiss, K.R., and Kupfermann, I. 1978. A neural pathway mediating satiation of feeding behavior in Aplysia. Behav. Biol. 23: 230-237.
50. -. 1987. Mechanisms underlying satiation of feeding behavior of the mollusc Aplysia. Behav. Neural. Biol. 48: 278-303.
51. Lamprecht, R., Hazvi, S., and Dudai, Y. 1997. cAMP response element-binding protein in the amygdala is required for long- but not short-term conditioned taste aversion memory. J. Neurosci. 17:8443-8450.
52. Lechner, H.A., Baxter, D.A., and Byrne, J.H. 2000a. Classical conditioning of feeding behavior in Aplysia: 1. Behavioral analysis. J. Neurosci. 20: 3369-3376.
53. -. 2000b. Classical conditioning of feeding behavior in Aplysia: 11. Neurophysiological correlates. J. Neurosci. 20: 3377-3386.
54. Lloyd, P.E., Kupfermann, I., and Weiss, K.R. 1988. Central peptidergic neurons regulate gut motility in Aplysia. J. Neurophysiol. 59: 1613-1626.
55. Lukowiak, K. and Sahley, C.L. 1981. The in vitro classical conditioning of the gill withdrawal reflex of Aplysia californica. Science 212: 1516-1518.
56. Maksimova, O.A. and Balaban, P.M. 1984. Neuronal correlates of aversive learning in command neurons for avoidance behavior of Helix lucorum L. Brain Res. 292: 139-149.
57. Maren, S. 2001. Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci. 24: 897-931.
58. Menzel, R. and Müller, U. 1996. Learning and memory in honeybees: From behavior to neural substrates. Annu. Rev. Neurosci. 19: 379-404.
59. Morgan, P.T., Jing, J., Vilim, F.S., and Weiss, K.R. 2001. Interneuronal and peptidergic control of motor pattern switching in Aplysia. J. Neurophysiol. 87: 49-61.
60. Morton, D.W. and Chiel, H.J. 1993a. In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia. J. Comp. Physiol. [A] 172: 17-32.
61. -. 1993b. The timing of activity in motor neurons that produce radula movements distinguishes ingestion from rejection in Aplysia. J. Comp. Physiol. [A] 173: 519-536.
62. Moyer, J.R., Thompson, L.T., and Disterhoft, J.F. 1996. Trace eyeblink conditioning increases CA1 excitability in a transient and learning specific manner. J. Neurosci. 16: 5536-5546.
63. Mozzachiodi, R., Baxter, D.A., Cleary, L.J., and Byrne, J.H. 2000. Afferent inputs to cerebral-buccal interneuron 2 (CB1-2) and its synaptic connections to B31/32 in Aplysia. Soc. Neurosci. Abstr. 26: 450.
64. Murphy, G.G. and Glanzman, D.L. 1997. Mediation of classical conditioning in Aplysia californica by long-term potentiation of sensorimotor synapses. Science 278: 467-471.
65. Nargeot, R., Baxter, D.A., and Byrne, J.H. 1997. Contingent-dependent enhancement of rhythmic motor pattern: An in vitro analog of operant conditioning. J. Neurosci. 17: 8093-8105.
66. -. 1999a. In vitro analog of operant conditioning in Aplysia. I. Contingent reinforcement modifies the functional dynamics of an identified neuron. J. Neurosci. 19: 2247-2260.
67. -. 1999b. In vitro analog of operant conditioning in Aplysia. II. Modifications of the functional dynamics of an identified neuron contribute to motor pattern selection. J. Neurosci. 19: 2261-2272.
68. Nargeot, R., Baxter, D.A., Patterson, G.W., and Byrne, J.H. 1999c. Dopaminergic synapses mediate neuronal changes in an analog of operant conditioning. J. Neurophysiol. 81: 1983-1987.
69. Ono, L.K. and McCaman, R.E. 1980. Identification of additional histaminergic neurons in Aplysia: Improvement of single cell isolation techniques for in tandem physiological and chemical studies. Neuroscience 5: 835-840.
70. Perrins, R. and Weiss, K.R. 1996. A cerebral central pattern generator in Aplysia and its connections with buccal feeding circuitry. J. Neurosci. 16: 7030-7045.
71. Plummer, M.R. and Kirk, M.D. 1990. Premotor neurons B51 and B52 in the buccal ganglia of Aplysia californica: Synaptic connections, effects on ongoing motor rhythms, and peptide modulation. J. Neurophysiol. 63: 539-558.
72. Rose, S.P. 2000. God's organism? The chick as a model system for memory studies. Learn. Mem. 7:1-17.
73. Rosen, S.C., Weiss, K.R., and Kupfermann, I. 1979. Response properties and synaptic connections of mechanoafferent neurons in cerebral ganglion of Aplysia. J. Neurophysiol. 42: 954-974.
74. Rosen, S.C., Weiss, K.R., Cohen, J.L., and Kupfermann, I. 1982. Interganglionic cerebral-buccal mechanoafferents of Aplysia: Receptive fields and synaptic connections to different classes of neurons involved in feeding behavior. J. Neurophysiol. 48: 271-288.
75. B, buccalin and myomodulin in different classes of mechanoafferent neurons in the cerebral ganglion of Aplysia. J. Neurosci. 9: 390-402.
76. Rosen, S.C., Teyke, T., Miller, M.W., Weiss, K.R., and Kupfermann, I. 1991. Identification and characterization of cerebral-to-buccal interneurons implicated in the control of motor programs associated with feeding in Aplysia. J. Neurosci. 11: 3630-3655.
77. Sahley, C.L. 1995. What we have learned from the study of learning in the leech. J. Neurobiol. 27: 434-445.
78. Sahley, C.L. and Crow, T. 1998. Invertebrate learning: Current perspectives. In Neurobiology of learning and memory (eds. J.L. Martinez Jr. and R.P. Kesner), pp. 177-209. Academic Press, New York.
79. Sahley, C.L., Martin, K.A., and Gelperin, A. 1990. Analysis of associative learning in the terrestrial mollusc Limax maximus. II. Appetitive learning. J. Comp. Physiol. [A] 167: 339-345.
80. Sahley, C.L., Boulis, M.N., and Schuman, B. 1994. Associative learning modifies the shortening reflex in the semi-intact leech Hirudo medicinalis: Effects of pairing, predictability and CS preexposure. Behav. Neurosci. 108: 340-346.
81. Sánchez, J.A.D. and Kirk, M.D. 2000. Short-term synaptic enhancement modulates ingestion motor programs of Aplysia. J. Neurosci. 20: RC85:1-7.
82. -. 2001. Cerebral-buccal pathways in Aplysia californica: Synaptic connections, cooperative interneuronal effects and feedback during buccal motor programs. J. Comp. Physiol. [A] 187: 801-815.
83. -. 2002. Ingestion motor programs of Aplysia are modulated by short-term synaptic enhancement in cerebral-buccal interneuron pathways. Invert. Neurosci. 4: 199-212.
84. Schafe, G.E., Nader, K., Blair, H.T., and LeDoux, J.E. 2001. Memory consolidation of Pavlovian fear conditioning: A cellular and molecular perspective. Trends Neurosci. 24: 540-546.
85. Schwarz, M. and Susswein, A.J. 1986. Identification of the neural pathway for reinforcement of feeding when Aplysia learn that food is inedible. J. Neurosci. 6: 1528-1536.
86. Staras, K., Kemenes, G., and Benjamin, P.R. 1999. Cellular traces of behavioral classical conditioning can be recorded at several specific sites in a simple nervous system. J. Neurosci. 19: 347-357.
87. Susswein, A.J. and Byrne, J.H. 1988. Identification and characterization of neurons initiating patterned activity in the buccal ganglia of Aplysia. J. Neurosci. 8: 2049-2061.
88. Susswein, A.J. and Schwarz, M. 1983. A learned change of response to inedible food in Aplysia. Behav. Neural. Biol. 39: 1-6.
89. Susswein, A.J., Weiss, K.R., and Kupfermann, I. 1984. Internal stimuli enhance feeding behavior in the mollusc Aplysia. Behav. Neural. Biol. 41: 90-95.
90. Susswein, A.J., Hurwitz, I., Thorne, R., Byrne, J.H., and Baxter, D.A. 2002. Mechanisms underlying fictive feeding in Aplysia: Coupling between a large neuron with plateau potentials activity and a spiking neuron. J. Neurophysiol. 87: 2307-2323.
91. Talk, A.C. and Matzel, L.D. 1996. Calcium influx and release from intracellular stores contribute differentially to activity-dependent neuronal facilitation in Hermissenda photoreceptors. Neurobiol. Learn. Mem. 66:183-197.
92. Thompson, R.F. and Kim, J.J. 1996. Memory systems in the brain and localization of a memory. Proc. Natl. Acad. Sci. 93: 13438-13444.
93. Walters, E.T. and Byrne, J.H. 1983. Associative condítioning of single sensory neurons suggests a cellular mechanism for learning. Science 219: 405-408.
94. Warman, E.N. and Chiel, H.J. 1995. A new technique for chronic single-unit extracellular recording in freely behaving animals using pipette electrodes. J. Neurosci. Methods 57: 161-169.
95. Welzl, H., D'Adamo, P., and Lipp, H.P. 2001. Conditioned taste aversion as a learning and memory paradigm. Behav. Brain. Res. 125: 205-213.
96. Xin, Y., Weiss, K.R., and Kupfermann, I. 1995. Distribution in the central nervous system of Aplysia of afferent fibers arising from cell bodies located in the periphery. J. Comp. Neurol. 359: 627-643.
97. Zar, J.H. 1999. Biostatistical analysis, 4th ed. Prentice Hall, Engelwood Cliffs, NJ.