Target-specific regulation of synaptic efficacy in the feeding central pattern generator of Aplysia: Potential substrates for behavioral plasticity?

Biological Bulletin

Volumn 210, Issue 3, 2006, Pages 215-229

  Díaz Ríos, Manuel ^a   Miller, Mark W ^a  

^a UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID;

ADAPTATION; BEHAVIORAL RESPONSE; FEEDING BEHAVIOR; SNAIL; SUBSTRATE;

ANIMAL; APLYSIA; ARTICLE; BIOLOGICAL MODEL; CELL MEMBRANE POTENTIAL; DRUG EFFECT; ELECTRIC CONDUCTIVITY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEEDING BEHAVIOR; HISTOLOGY; INTERNEURON; METABOLISM; MOTONEURON; NERVE CELL PLASTICITY; PHYSIOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; APLYSIA; ELECTRIC CONDUCTIVITY; EXCITATORY POSTSYNAPTIC POTENTIALS; FEEDING BEHAVIOR; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; MOTOR NEURONS; NEURONAL PLASTICITY; SYNAPSES; SYNAPTIC TRANSMISSION;

APLYSIA;

EID: 33745728985     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/4134559     Document Type: Article

References (95)

1. Abraham, W. C., and M. F. Bear. 1996. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19: 126-130.
2. Angstadt, J. D., and R. L. Calabrese. 1989. A hyperpolarization-activated inward current in heart interneurons of the medicinal leech. J. Neurosci. 9: 2846-2857.
3. Atwood, H. L. 1967. Variation in physiological properties of crustacean motor synapses. Nature 215: 57-58.
4. Balaban, P. M. 2002. Cellular mechanisms of behavioral plasticity in terrestrial snail. Neurosci. Biobehav. Rev. 26: 597-630.
5. Benjamin, P. R., K. Staras, and G. Kemenes. 2000. A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn. Mem. 7: 124-131.
6. Bettler, B., K. Kaupmann, J. Mosbacher, and M. Gassmann. 2004. Molecular structure and physiological functions of GABA(B) receptors. Physiol. Rev. 84: 835-867.
7. Bittner, G. D. 1968. Differentiation of nerve terminals in the crayfish opener and its functional significance. J. Gen. Physiol. 51: 731-758.
8. Brembs, B., F. D. Lorenzetti, F. D. Reyes, D. A. Baxter, and J. H. Byrne. 2002. Operant reward learning in Aplysia: neuronal correlates and mechanisms. Science 296: 1706-1709.
9. Brembs, B., D. A. Baxter, and J. H. Byrne. 2004. Extending in vitro conditioning in Aplysia to analyze operant and classical processes in the same preparation. Learn. Mem. 11: 412-420.
10. Brezina, V., I. V. Orekhova, and K. R. Weiss. 2003a. Neuromuscular modulation in Aplysia. I. Dynamic model. J. Neurophysiol. 90: 2592-2612.
11. Brezina, V., I. V. Orekhova, and K. R. Weiss. 2003b. Neuromuscular modulation in Aplysia. II. Modulation of the neuromuscular transform in behavior. J. Neurophysiol. 90: 2613-2628.
12. Byrne, J. H., and E. R. Kandel. 1996. Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 16: 425-435.
13. Carew, T. J., and E. R. Kandel. 1974. Synaptic analysis of the interrelationships between behavioral modifications in Aplysia. Pp. 339-383 in Synaptic Transmission and Neuronal Interaction, M. V. L. Bennett, ed. Raven Press, New York.
14. Church, P. J., and P. E. Lloyd. 1994. Activity of multiple identified motor neurons recorded intracellularly during evoked feeding-like motor programs in Aplysia. J. Neurophysiol. 72: 1794-1809.
15. Cohen, J. L., K. R. Weiss, and I. Kupfermann. 1978. Motor control of buccal muscles in Aplysia. J. Neurophysiol. 41: 157-180.
16. Colwill, R., K. Goodrum, and A. Martin. 1997. Pavlovian appetitive discriminative conditioning in Aplysia californica. Anim. Learn. Behav. 25: 268-276.
17. Cropper, E. C., P. E. Lloyd, W. Reed, R. Tenenbaum, I. Kupfermann, and K. R. Weiss. 1987. Multiple neuropeptides in cholinergic motor neurons of Aplysia: evidence for modulation intrinsic to the motor circuit. Proc. Natl. Acad. Sci. USA 84: 3486-3490.
18. Cropper, E. C., I. Kupfermann, and K. R. Weiss. 1990. Differential firing patterns of the peptide-containing cholinergic neurons B15 and B16 during feeding behavior in Aplysia. Brain Res. 522: 176-179.
19. Cropper, E. C., C. G. Evans, I. Hurwitz, J. Jing, A. Proekt, A. Romero, and S.C. Rosen. 2004. Feeding neural networks in the mollusk Aplysia. Neurosignals 13: 70-86.
20. del Castillo, J., and B. Katz. 1954. Statistical factors involved in neuromuscular facilitation and depression. J. Physiol. (Lond.) 124: 574-585.
21. Díaz-Ríos, M., and M. W. Miller. 2002. GABA and dopamine colocalization in interneurons of the Aplysia feeding circuit: presynaptic actions of GABA. Abstract 367.12. [Online: 2002 Abstract Viewer/Itinerary Planner]. Society for Neuroscience, Washington, DC.
22. Díaz-Ríos, M., and M. W. Miller. 2005. Rapid dopaminergic signaling by interneurons that contain markers for catecholamines and GABA in the feeding circuitry of Aplysia. J. Neurophysiol. 93: 2142-2156.
23. Díaz-Ríos, M., E. Suess, and M. W. Miller. 1999. Localization of GABA-like immunoreactivity in the central nervous system of Aplysia californica. J. Comp. Neurol. 413: 255-270.
24. Díaz-Ríos, M., E. Oyola, and M. W. Miller. 2002. Colocalization of γ-aminobutyric acid-like immunoreactivity and catecholamines in the feeding network of Aplysia californica. J. Comp. Neurol. 445: 29-46.
25. Due, M. R., J. Jing, and K. R. Weiss. 2004. Dopaminergic contributions to modulatory functions of a dual-transmitter interneuron in Aplysia. Neurosci. Lett. 358: 53-57.
26. Fischer, T. M., T. E. J. Blazis, N. A. Priver, and T. J. Carew. 1997. Metaplasticity at identified inhibitory synapses in Aplysia. Nature 389: 860-865.
27. Fisher, S. A., T. M. Fischer, and T. J. Carew. 1997. Multiple overlapping processes underlying short-term synaptic enhancement. Trends Neurosci. 20: 170-177.
28. Gardner, D., and E. R. Kandel. 1977. Physiological and kinetic properties of cholinergic receptors activated by multiaction interneurons in buccal ganglia of Aplysia. J. Neurophysiol. 40: 333-348.
29. Glanzman, D. L. 1995. The cellular basis of classical conditioning in Aplysia californica: It's less simple than you think. Trends Neurosci. 18: 30-36.
30. Golowasch, J., and E. Marder. 1992. Ionic currents of the lateral pyloric neuron of the stomatogastric ganglion of the crab. J Neurophysiol. 67: 318-331.
31. Gutovitz, S., J. T. Birmingham, J. A. Luther, D. J. Simon, and E. Marder. 2001. GABA enhances transmission at an excitatory glutamatergic synapse. J. Neurosci. 21: 5935-5943.
32. Harris-Warrick, R. M., and E. Marder. 1991. Modulation of neural networks for behavior. Annu. Rev. Neurosci. 14: 39-57.
33. Hawkins, R. D., E. R. Kandel, and S. A. Siegelbaum. 1993. Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu. Rev. Neurosci. 16: 625-665.
34. Hurwitz, I., I. Kupfermann, and K. R. Weiss. 2003. Fast synaptic connections from CBIs to pattern-generating neurons in Aplysia: initiation and modification of motor programs. J. Neurophysiol. 89: 2120-2136.
35. Jing, J., and K. R. Weiss. 2001. Neural mechanisms of motor program switching in Aplysia. J. Neurosci. 21: 7349-7362,
36. Jing, J., and K. R. Weiss. 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.
37. Jing, J., F. S. Vilim, J.-S. Wu, J.-H. Park, and K. R. Weiss. 2003. Concerted GABAergic actions of Aplysia feeding interneurons in motor program specification. J. Neurosci. 23: 5283-5294.
38. Jordan, R., K. P. Cohen, and M. D. Kirk. 1993. Control of intrinsic buccal muscles by motoneurons B11, B15, and B16 in Aplysia californica. J. Exp. Zool. 265: 496-506.
39. Kabotyanski, E. A., D. A. Baxter, and J. H. Byrne. 1998. Identification and characterization of catecholaminergic neuron B65 that initiates and modifies patterned activity in the buccal ganglion of Aplysia. J. Neurophysiol. 79: 605-621.
40. Handel, E. R., and J. H. Schwartz. 1982. Molecular biology of learning: modulation of transmitter release. Science 218: 433-443.
41. Kandel, E. R., and L. Tauc. 1966. Anomalous rectification in the metacerebral giant cells and its consequences for synaptic transmission. J. Physiol. 183: 287-304.
42. Katz, P. S., ed. 1999. Beyond Neurotransmission: Neuromodulation and Its Importance for Information Processing. Oxford University Press. New York.
43. Katz, P. S., and W. N. Frost. 1996. Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci. 19: 54-61.
44. Katz, P. S., M. D. Kirk, and C. K. Govind. 1993. Facilitation and depression at different branches of the same motor axon: evidence for presynaptic differences in release. J. Neurosci. 13: 3075-3089.
45. Katz, P. S., P. A. Getting, and W. N. Frost. 1994. Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature 367: 729-731.
46. Klein, A. N., K. R. Weiss, and E. C. Cropper. 2000. Glutamate is the fast excitatory neurotransmitter of small cardioactive peptide-containing Aplysia radula mechanoafferent neuron B21. Neurosci. Lett. 289: 37-40.
47. Kovac, M. P., E. M. Matera, P. J. Volk, and W. J. Davis. 1986. Food avoidance learning is accompanied by synaptic attenuation in identified interneurons controlling feeding behavior in Pleurobranchaea. J. Neurophysiol. 56: 891-905.
48. Krasne, F. B. 1978. Extrinsic control of intrinsic neuronal plasticity: an hypothesis from work on simple systems. Brain Res. 140: 197-216.
49. Kupfermann, I. 1974. Feeding behavior in Aplysia: a simple system for the study of motivation. Behav. Biol. 10: 1-26.
50. Kupfermann, I. 1979. Modulatory actions of neurotransmitters. Annu. Rev. Neurosci. 2: 447-465.
51. Kupfermann, I. 1991. Functional studies of cotransmission. Physiol. Rev. 71: 683-732.
52. Kupfermann, I., J. L. Cohen, D. E. Mandelbaum, M. Schonberg, A. J. Susswein, and K. R. Weiss. 1979. Functional role of serotonergic neuromodulation in Aplysia. Fed. Proc. 38: 2095-2102.
53. Kupfermann, I., S. Rosen, T. Teyke, E. C. Cropper, M. Miller, F. Vilim, and K. R. Weiss. 1989. Neurobiology of behavioral states in Aplysia: non-associative forms of plasticity of feeding responses. Pp. 47-59 in Dynamics and Plasticity in Neuronal Systems. N. Elsner, and W. Winger, eds. Georg Thieme Verlag, New York.
54. Lechner, H. A., D. A. Baxter, and J. H. Byrne. 2000a. Classical conditioning of feeding in Aplysia. I. Behavioral analysis. J. Neurosci. 20: 3369-3376.
55. Lechner, H. A., D. A. Baxter, and J. H. Byrne. 2000b. Classical conditioning of feeding in Aplysia. II. Neurophysiological correlates. J. Neurosci. 20: 3377-3386.
56. Liao, X., and E. T. Walters. 2002. The use of elevated divalent cation solutions to isolate monosynaptic components of sensorimotor connections in Aplysia. J. Neurosci. Meth. 120: 45-54.
57. Marder, E. 1998. From biophysics to models of network function. Annu. Rev. Neurosci. 21: 25-45.
58. Martin, A. R. 1955. A further study of the statistical composition on the end-plate potential. J. Physiol. 130: 114-122.
59. Martin, K. C., M. Barad, and E. R. Kandel. 2000. Local protein synthesis and its role in synapse-specific plasticity. Curr. Opin. Neurobiol. 10: 587-592.
60. Menzel, R. 2001. Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 8: 53-62.
61. Miwa, A., M. Ui, and N. Kawai. 1990. G protein is coupled to presynaptic glutamate and GABA receptors in lobster neuromuscular synapse. J. Neurophysiol. 63: 173-180.
62. Morgan, P. T., R. Perrins, P. E. Lloyd, and K. R. Weiss. 2000. Intrinsic and extrinsic modulation of a single central pattern generating circuit. J. Neurophysiol. 84: 1186-1193.
63. Morgan, P. T., J. Jing, F. S. Vilim, and K. R. Weiss. 2002. Interneuronal and peptidergic control of motor pattern switching in Aplysia. J. Neurophysiol. 87: 49-61.
64. Morielli, A. D., E. M. Matera, M. P. Kovac, R. G. Shrum, K. J. McCormack, and W. J. Davis. 1986. Cholinergic suppression: a postsynaptic mechanism of long-term associative learning. Proc. Natl. Acad. Sci. USA 83: 4556-4560.
65. Morton, D. W., and H. J. Chiel. 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.
66. Morton, D. W., and H. J. Chiel. 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.
67. Mozzachiodi, R., H. A. Lechner, D. A. Baxter, and J. H. Byrne. 2003. In vitro analog of classical conditioning of feeding in Aplysia. Learn. Mem. 10: 478-494.
68. Nadim, F., and Y. Manor. 2000. The role of short-term synaptic dynamics in motor control. Curr. Opin. Neurobiol. 10: 683-690.
69. Nargeot, R., D. A. Baxter, and J. H. Byrne. 1997. Contingent-dependent enhancement of rhythmic motor patterns: an in vitro analog of operant conditioning. J. Neurosci. 17: 8093-8105.
70. Nargeot, R., D. A. Baxter, and J. H. Byrne. 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.
71. Nargeot, R., D. A. Baxter, and J. H. Byrne. 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.
72. Newlin, S. A., W. T. Schlapfer, and S. H. Barondes. 1980. Separate serotonin and dopamine receptors modulate the duration of post-tetanic potentiation at an Aplysia synapse without affecting other aspects of synaptic transmission. Brain Res. 181:107-125.
73. Nusbaum, M. P., D. M. Blitz, A. M. Swensen, D. Wood, and E. Marder. 2001. The roles of co-transmission in neural network modulation. Trends Neurosci. 24:146-154.
74. Parker, D., and S. Grillner. 1999. Activity-dependent metaplasticity of inhibitory and excitatory synaptic transmission in the lamprey spinal cord locomotor network. J. Neurosci. 19:1647-1656.
75. Parker, D., and S. Grillner. 2000. The activity-dependent plasticity of segmental and intersegmental synaptic connections in the lamprey spinal cord. Eur. J. Neurosci. 12: 2135-2146.
76. B receptors in the opener neuromuscular junction of crayfish. J. Neurophysiol. 81: 1184-1191.
77. Philippe, E., G. Grenon, and J. P. Tremblay. 1981. Baclofen modifies via the release of monoamines the synaptic depression, frequency facilitation, and posttetanic potentiation observed at an identified cholinergic synapse of Aplysia californica. Can. J. Physiol. Pharmacol. 59: 244-252.
78. Proekt, A., V. Brezina, and K. R. Weiss. 2004. Dynamical basis of intentions and expectations in a simple neuronal network. Proc. Natl. Acad. Sci. USA 101: 9447-9452.
79. Rosen, S. C., K. R. Weiss, R. S. Goldstein, and I. Kupfermann. 1989. The role of a modulatory neuron in feeding and satiation in Aplysia: effects of lesioning of the serotonergic metacerebral cells. J. Neurosci. 9: 1562-1578.
80. Sakurai, A., and P. S. Katz. 2003. Spike timing-dependent serotonergic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. J. Neurosci. 23: 10745-10755.
81. Sánchez, J. A., and M. D. Kirk. 2000. Short-term enhancement modulates ingestion motor programs of Aplysia. J. Neurosci. 20: RC85.
82. Sánchez, J. A., and M. D. Kirk. 2002. Ingestion motor programs of Aplysia are modulated by short-term synaptic enhancement in cerebral-buccal interneuron pathways. Invertebr. Neurosci. 4: 199-212.
83. Staras, K., G. Kemenes, and P. R. Benjamin. 1999. Cellular traces of behavioral classical conditioning can be recorded at several specific sites in a simple nervous system. J. Neurosci. 19: 347-357.
84. Straub, V. A., B. J. Styles, J. S. Ireland, M. O'Shea, and P. R. Benjamin. 2004. Central localization of plasticity involved in appetitive conditioning in Lymnaea. Learn. Mem. 11: 787-793.
85. Susswein, A. J., and M. Schwarz. 1983. A learned change of response to inedible food in Aplysia. Behav. Neural. Biol. 39:1-6.
86. Svensson, E., A. Proekt, and K. R. Weiss. 2004. Complementary effects of co-localized dopamine and GABA on synaptic transmission in the Aplysia feeding network. Abstract 537.4. [Online: 2004 Abstract Viewer/Itinerary Planner], Society for Neuroscience, Washington, DC.
87. Sweedler, J. V., L. Li, S. S. Rubakhin, V. Alexeeva, N. C. Dembrow, O. Dowling, J. Jing, K. R. Weiss, and F. S. Vilim. 2002. Identification and characterization of the feeding circuit-activating peptides, a novel neuropeptide family of Aplysia. J. Neurosci. 22: 7797-7808.
88. Teyke, T., S. C. Rosen, K. R. Weiss, and I. Kupfermann. 1993. Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry of Aplysia. Brain Res. 630: 226-237.
89. Tremblay, J. P., P. B. Woodson, W. T. Schlapfer, and S. H. Barondes. 1976. Dopamine, serotonin and related compounds: presynaptic effects on synaptic depression, frequency facilitation, and post-tetanic potentiation at a synapse in Aplysia californica. Brain Res. 109: 61-81.
90. Weiss, K. R., V. Brezina, E. C. Cropper, S. L. Hooper, M. W. Miller, W. C. Probst, F.S. Vilim, and I. Kupfermann. 1992. Peptidergic cotransmission in Aplysia: functional implications for rhythmic behaviors. Experientia 48: 456-463.
91. Woodson, P. B., J. P. Tremblay, W. T. Schlapfer, and S. H. Barondes. 1976. Inhibition modifies the presynaptic plasticities of the transmission process at the synapse in Aplysia californica. Brain Res. 109: 83-95.
92. Ye, H., D. W. Morton, and H. J. Chiel. 2006. Neuromechanics of coordination during swallowing in Aplysia californica. J. Neurosci. 26: 1470-1485.
93. Yuste, R., J. N. MacLean, J. Smith, and A. Lansner. 2005. The cortex as a central pattern generator. Nature Rev. Neurosci. 6: 477-483.
94. Zhurov, Y., A. Proekt, K. R. Weiss, and V. Brezina. 2005. Changes of internal state are expressed in coherent shifts of neuromuscular activity in Aplysia feeding behavior. J. Neurosci. 25: 1268-1280.
95. Zucker, R. S., and W. G. Regehr. 2002. Short-term synaptic plasticity. Annu. Rev. Physiol. 64: 355-405.