In vitro analog of operant conditioning in Aplysia. I. Contingent reinforcement modifies the functional dynamics of an identified neuron

Journal of Neuroscience

Volumn 19, Issue 6, 1999, Pages 2247-2260

  Nargeot, Romuald ^a,b   Baxter, Douglas A ^a   Byrne, John H ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Aplysia californica; B51; Buccal ganglia; Central pattern generator; Contingent reinforcement; Learning and memory; Neuronal dynamics; Operant conditioning; Regenerative properties

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; APLYSIA; ARTICLE; INSTRUMENTAL CONDITIONING; MEMORY CONSOLIDATION; MOTOR ACTIVITY; NERVE CELL MEMBRANE CONDUCTANCE; NERVE EXCITABILITY; NERVE FUNCTION; NERVE POTENTIAL; NERVE REGENERATION; NERVE STIMULATION; NONHUMAN; PATTERN GENERATOR; PATTERN STIMULATION; PRIORITY JOURNAL; REINFORCEMENT; STATE DEPENDENT LEARNING;

EID: 0033559464     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-06-02247.1999     Document Type: Article

References (102)

1. Bal T. Nagy F. Moulins M (1994) Muscarinic modulation of a patterngenerating network: control of the neuronal properties. J Neurosci 14:3019-3035.
2. Baxter DA, Nargeot R. Patterson GW. Byrne JH (1948) A dopaminc antagonist (ergonovine) impaired the enhancement of motor patterns by contingent reinforcement in the isolated huccal ganglia of Aplysia. Soc Neurosei Abstr 24:1891.
3. Beggs JM. Brown TH. Byrnc JH, Crow T. LeDouz JE. LeBar K, Thompson RF (1998) Learning anil memory: basic mechanisms. In: Fundamental neuroscience (Zigmond MJ. Bloom FE. Landis SC. Roberts JL. Squire LR. eds), pp 1411-1454. San Diego: Academic.
4. Bianehi AL, Denavit-Suubic M, Champagnat J (1995) Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. Physiol Rev 75:1-45.
5. Booker R.Quinn WG (1981) Conditioning of leg position in normal and mutant Drosopliila. Proc Natl Acad Sci USA 78:3940-3944.
6. Brons JF, Woody CD (1980) Long-term changes in excitability of cortical neurons after Pavlovian conditioning and extinction. J Ncurophysiol 44:605-615.
7. Byrne JH (1987) Cellular analysis of associative learning. Physiol Rev 67:329-439.
8. Byrne JH. Zwartjes R, Homayouni R. Crilz SD, Eskin A (1993) Roles of second messenger pathways in neuronal plasticity and in learning and memory. Adv Second Messenger Phosphoprotein Res 27:47-108.
9. Canavier'cC. Butera RJ, Dror RO, Baxter DA, Clark JW, Byrne JH (1997) Phase response characteristics of model neurons determine which patterns arc expressed in a ring circuit model of gait generation. Biol Cybern 77:367-380.
10. Carew TJ. Sahlcy CL (1986) Invertebrate learning and memory: from behavior to molecules. Annu Rev Neurosci 9:435-487.
11. Carp JS, Wolpaw JR ( 1994) Motoneuron plasticity underlying operantly conditioned decrease in primate H-reflex. J Neurophysiol 72:431-442.
12. Cazalets J-R, Nagy F, Moulins M (1990) Suppressive control of the crustacean pylorie network by a pair of identified interneurons. II. Modulation of the neuronal properties. J Neurosci 10:458-468.
13. Church PJ. Lloyd PE (1991) Expression of diverse neuropeptidc cotransmitters by identified motor neurons in Aplvsia. J Neurosci 11:618-625.
14. Church PJ, Lloyd PE (1994) Activity of multiple identified motor neurons recorded intracellularly during evoked feeding like motor programs in Aplysia. J Neurophysiol 72:1794-1809.
15. Church PJ, Cohen KP. Scott'ML. Kirk MD (1991) Peptidergic motoncurons in the buccal ganglia of Aplysia californien: immunocytochemical, morphological and physiological characterizations. J Comp Physiol [A] 168:323-336.
16. Colwill RM. Goodrum K. Martin A (1997) Pavlovian appetitive discriminative conditioning in Aplysia californien. Anim Learn Behav 25:268-276.
17. Cook DG, Carew TJ (1986) Operant conditioning of head-waving in Aplysia. Proc Natl Acad Sci USA 83:1120-1124.
18. Cropper EC, Kupfermann I, Wciss KR (1990) Differential firing patterns of the peptide-containingcholinergic motor neurons B15 and B16 during feeding behavior in Aplysia. Brain Res 522:176-179.
19. Crow TJ, Alkon DL (1980) Associative behavioral modification in Hermissrnda: cellular correlates. Science 209:412-414.
20. Delcomyn F (1980) Neuronal basis of rhythmic behavior in animals. Science 210:492-498.
21. Dickinson PS. Moulins M ( 1992) Interactions and combinations between different networks in the stomatogastric nervous system. In: Dynamic biological networks (Harris-Warrick RM, Marder E, Selverston AI, Moulins M, eds). pp 139-160. Cambridge, MA: MIT.
22. Dickinson PS, Nagy F (1983) Control of a central pattern generator by an identified modulatory intcrneuronc in Crustacea. II. Induction and suppression of plateau properties in pyloric neurones. J Exp Biol 105:59-82.
23. Dickinson PS, Mecsas C, Marder E (1990) Neuropeptide fusion of two motor-pattern generator circuits. Nature 344:155-158.
24. Disterhoft JF, Coulter DA, Alkon DL (1986) Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc Natl Acad Sci USA 83:2733-2737.
25. Evans CG, Cropper EC (1998) Proprioceptive input to feeding motor programs in Aplysia. J Neurosci 18:8016-8031.
26. Feng-Chen KC, Wolpaw JR (1996) Operant conditioning of H-reflex changes synaptic terminals on primate motoneurons. Proc Natl Acad Sci USA 93:9206-9211.
27. Fitzgerald KK, Takacs CA, Carew TJ (1997) Nonassociative and associative modification of head-waving produced by aversive tentacular stimuli in Aplysia. Learn Mem 3:366-375.
28. Friesen WO, Poon M, Stent GS (1976) An oscillatory neuronal circuit generating a locomotor rhythm. Proc Natl Acad Sci USA 73:3734-3738.
29. Getting PA (1989) Emerging principles governing the operation of the neural networks. Annu Rev Neurosci 12:185-204.
30. Getting PA, Dekin MS (1985) Tritonia swimming: a model system for integration within rhythmic motor systems. In: Model neural networks and behavior (Selverston AI, ed), pp 3-20. New York: Plenum.
31. Green CS, Soffe SR (1996) Transitions between two different motor patterns in Xenopus embryos. J Comp Physiol [A] 178:279-291.
32. Grillner S (1985) Neurobiological bases of rhythmic motor acts in invertebrates. Science 228:143-149.
33. Grillner S, Georgopoulos AP, Jordan LM (1997) Selection and initiation of motor behavior. In: Neurons, networks, and motor behavior (Stein PSG, Grillner S, Selverston AI, Stuart DG, eds), pp 3-19. Cambridge, MA: MIT.
34. Harris-Warrick RM, Marder E (1991) Modulation of neuronal network for behavior. Annu Rev Neurosci 14:39-57.
35. Hawkins R. Clark G, Kandel ER (1985) Operant conditioning and differential classical conditioning of gill withdrawal in Aplysia. Soc Neurosci Abstr 11:796.
36. Heinzel H-G (1988) Gastric mill activity in the lobster. I. Spontaneous modes of chewing. J Neurophysiol 59:528-550.
37. Hooper SL. Moulins M (1989) Switching of a neuron from one network to another by sensory-induced changes in membrane properties. Science 244:1587-1589.
38. Hooper SL, Moulins M, Nonnotte L (1990) Sensory input induces longlasting changes in the output of the lobster pyloric network. J Neurophysiol 64:1555-1573.
39. Horridge GA (1962) Learning of leg position by headless insects. Nature 193:697-698.
40. Hoyle G (1979) Mechanisms of simple motor learning. Trends Neurosci 2:153-155.
41. Hoyle G (1980) Learning, using natural reinforcement, in insect preparations that permit cellular neuronal analysis. J Neurobiol 11:323-354.
42. Hoyle G (1982) Pacemaker change in a learning paradigm. In: Cellular pacemaker (Carpenter DO, ed), pp 3-25. New York: Wiley.
43. Hultborn H, Kiehn O (1992) Neuromodulation of vertebrate motor neuron membrane properties. Curr Opin Neurobiol 2:770-775.
44. Hurwitz I, Susswein AJ (1996) B64. a newly-identified central pattern generator element producing a phase switch from protraction to retraction in buccal motor programs of Aplysia californien. J Neurophysiol 75:1327-1344.
45. Hurwitz I, Neustadter D, Morton DW, Chiel HJ, Susswein AJ (1996) Activity patterns of the B31/32 pattern initiators innervating the 12 muscle of the buccal mass during normal feeding movements mAplysia californien. J Neurophysiol 75:1309-1326.
46. Hurwitz I, Kupfermann I, Susswein AJ (1997) Different roles of neurons B63 and B34 that are active during the protraction phase of the buccal motor programs in Aplysia californien. J Neurophysiol 78:1305-1319.
47. Jaeger BJ, Olivares SA, Wetzel MC (1987) Operant conditioning in relation to natural EMG during rapid human walking. Am J Phys Med 66:59-76.
48. Jaffard R, Jeantet Y (1981) Posttraining changes in excitability of the commissural path-CAl pyramidal cell synapse in the hippocampus of mice. Brain Res 220:167-172.
49. Jaffard R, Destrade C, Soumireu-Mourat B, Durkin T, Ehel A (1980) Changes in hippocampal cholincrgic activity following learning in mice. Neurosci Lett 19:349-352.
50. Kandel ER, Schwartz JH (1982) Molecular biology of learning: modulation of transmitter release. Science 218:433-443.
51. Katz PS, Harris-Warrick RM (1991) Recruitment of crab gastric mill neurons into the pyloric motor pattern by mechanosensory afferent stimulation. J Neurophysiol 65:1442-1451.
52. Kiehn O (1991) Plateau potentials and active integration in the "final common pathway" for motor behavior. Trends Neurosci 14:68-73.
53. Konorski J (1948) Conditioned reflexes and neuronal organization. Cambridge, UK: Cambridge UP.
54. Kupfermann I (1974a) Feeding behavior in Aplysia: a simple system for the study of motivation. Bchav Biol 10:1-26.
55. Kupfermann I (1974b) Dissociation of the appetitive and consummatory phases of feeding behavior in Aplysia: a lesion study. Behav Biol 10:89-97.
56. Lechner HA, Baxter DA, Byrne JH (1997) Classical conditioning of feeding in Aplysia. Soc Neurosci Ahstr 23:1334.
57. Levitan ES, Lcvitan IB (1988) Serotonin acting via cyclic AMP enhances both the hypcrpolarizing and depolarizing phases of bursting pacemaker activity in the Aplysia neuron R15. J Neurosci 8:1152-1161.
58. Llinas R (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242:1654-1664.
59. Llinas R, Yarom Y (1986) Oscillatory properties of guinea pig inferior olivary neurons and their pharmacological modulation: an in vitro study. J Physiol (Lond) 376:163-182.
60. Lukowiak K. Ringseis E, Spencer G, Wildcring W, Naweed S (1996) Operant conditioning of the aerial respiratory behavior in Lymnaea stagnate. J Exp Biol 199:683-691.
61. Lydie R (1989) Central pattern-generating neurons and the search for general principles. FASEB J 3:2457-2468.
62. Mahajan DS, Desiraju T (1988) Alterations of dendritic branching and spine densities of hippocampal CA3 pyramidal neurons induced by operant conditioning in the phase of brain growth spurt. Exp Neurol 100:1-15.
63. Maier SF (1989) Learned helplessness: event covariation and cognitive changes. In: Contemporary learning theories (Klein SB, Mowrer RR, eds), pp 73-110. Hillsdale, NJ: LEA.
64. Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687-717.
65. Marder E, Abbott LF, Turrigiano GG, Liu Z, Golowasch J (1996) Memory from the dynamics of intrinsic membrane currents. Proc Natl Acad Sci USA 93:13481-13486.
66. McClellan AD (1982) Movements and motor patterns of the buccal mass of Pleurobranchaea during feeding, regurgitation and rejection. J Exp Biol 98:213-228.
67. Meyrand P, Simmers J, Moulins M (1991) Construction of a patterngenerating circuit with neurons of different networks. Nature 351:60-63.
68. Meyrand P, Simmers J, Moulins M (1994) Dynamic construction of a neural network from multiple pattern generators in the lobster stomatogastric nervous system. J Neurosci 14:630-644.
69. Miller NE (1969) Learning of visceral and glandular responses. Science 163:434-445.
70. Mortin LI, Keifer J, Stein PSG (1985) Three forms of the scratch reflex in the spinal turtle: movement analyses. J Neurophysiol 53:1501-1516.
71. Morton DW, Chiel HJ (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.
72. Morton DW, Chiel HJ (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.
73. Nargeot R, Moulins M (1997) Sensory-induced plasticity of motor pattern selection in the lobster stomatogastric nervous system. Eur J Neurosci 9:1636-1645.
74. Nargeot R, Baxter DA, Byrne JH (1997a) Dynamic recruitment of neurons into the central pattern generator (CPG) for feeding is associated with motor pattern selection in Aplysia. Soc Neurosci Abstr 23:1046.
75. Nargeot R, Baxter DA, Byrne JH (1997b) Contingent-dependent enhancement of rhythmic motor patterns: an in vitro analog of operant conditioning. J Neurosci 17:8093-8105.
76. Nargeot R. Baxter DA, Byrne JH (1998) Contingent reinforcement in an analogue of operant conditioning modified the intrinsic membrane properties of an identified Aplysia neuron (B51). Soc Neurosci Ahstr 24:1890.
77. Nargeot R, Baxter DA. Byrne JH (1999a) In vitro analog of operant conditioning in Aplvsia. II. Modifications of the functional dynamics of an identified neuron contribute to motor pattern selection. J Neurosci 19:2261-2272.
78. Nargeot R. Baxter DA, Patterson GW. Byrne JH (1999b) Dopaminergic synapses mediate neuronal changes in an analogue of operant conditioning. J Neurophysiol. in press.
79. Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16:265-297.
80. Plummer MR, Kirk MD (1990) Premotor neurons B51 and B52 in the buccal ganglia of Aplvsia californien: synaptic connections, effect on ongoing motor rhythms, and peptide modulation. J Neurophysiol 63:539-558.
81. Rossignol S, Dubuc R (1994) Spinal pattern generation. Curr Opin Neurobiol 4:894-902.
82. Russell DF. Hartline DK (1978) Bursting neural networks: a rcexamination. Science 200:453-456.
83. Russo RE. Hounsgaard J (1996) Plateau generating neurones in the dorsal horn in an in vitro preparation of the turtle spinal cord. J Physiol (Lond) 493:39-54.
84. Schulz H (1987) One-trial instrumental conditioning in rats. Acta Physiol Hung 70:111-115.
85. Selverston AI, Moulins M (1985) Oscillatory neural networks. Annu Rev Physiol 47:29-48.
86. Skelton W, Scarth AS, Wilkie DM, Miller JJ, Phillips AG (1987) Long-term increases in dentate granule cell responsivity accompany operant conditioning. J Neurosci 7:3081-3087.
87. Skinner BF (1938) The behavior of organisms: an experimental analysis. New York: Appleton-Century-Crofts.
88. Skinner BF (1966) The phylogeny and ontogeny of behavior: contingencies of reinforcement throw light on contingencies of survival in the evolution of behavior. Science 153:1205-1213.
89. Skinner BF (1981) Selection by consequences. Science 213:501-504.
90. Spencer G, Inoue I, Cotter R. Syed N. Lukowiak K (1996) Alterations in synaptic activity to and within a CPG may underlie the operant conditioning of aerial respiratory behaviour in Lymnaea. Soc Neurosci Abstr 22:1404.
91. Susswcin AJ. Byrne JH (1988) Identification and characterization of neurons initiating patterned neural activity in the buccal ganglia of Aplysia. i Neurosci 8:2049-2061.
92. Susswein AJ. Schwarz M, Feldman E (1986) Learned changes of feeding behavior in Aplvsia in response to edible and inedible foods. J Neurosci 6:1513-1527.
93. Thompson RF ( 1988) The neuronal basis of basic associative learning of discrete behavioral responses. Trends Neurosci 11:152-155.
94. Thorndike EL (1911) Animal intelligence: experimental studies. New York: Macmillan.
95. Thorndike EL (1933) A proof of the law of effect. Science 77:173-175.
96. Turrigiano G, Abbott LF. Marder E (1994) Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264:974-977.
97. Walters ET. Byrnc JH, Carew TJ, Kandel ER (1983) Mcchanoafferent neurons innervating tail of Aplysia. II. Modulation by sensitizing stimulation. J Neurophysiol 50:1543-1559.
98. WeimannJM, Marder E (1994) Switching neurons are integral members of multiple oscillatory networks. Curr Biol 4:896-902.
99. Wolpaw JR (1987) Operant conditioning of primate spinal reflexes: the H-reflex. J Neurophysiol 57:443-459.
100. Wolpaw JR (1997) The complex structure of a simple memory. Trends Neurosci 20:588-594.
101. Woollacott M, Hoyle G (1977) Neural events underlying learning in insects: changes in pacemaker. Proc R Soc Lond B Biol Sci 195:395-415.
102. Zar JH (1996) Biostatistical analysis, Ed 3. Englewood Cliffs. NJ: Prentice-Hall.