Neural mechanisms of operant conditioning and learning-induced behavioral plasticity in Aplysia

Cellular and Molecular Life Sciences

Volumn 68, Issue 5, 2011, Pages 803-816

  Nargeot, Romuald ^a   Simmers, John ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Aplysia; Central pattern generator; Endogenous bursting; Feeding; Learning; Operant conditioning; Synaptic plasticity

Indexed keywords

ANIMAL BEHAVIOR; APLYSIA; AVERSION; DECISION MAKING; DEPOLARIZATION; DOPAMINE BRAIN LEVEL; FEEDING BEHAVIOR; INSTRUMENTAL CONDITIONING; LEARNING; MEMBRANE CONDUCTANCE; MOTOR PERFORMANCE; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; REINFORCEMENT; REVIEW; REWARD; SENSORIMOTOR INTEGRATION; STATE DEPENDENT LEARNING; SYNAPTIC TRANSMISSION;

ANIMALS; APLYSIA; CONDITIONING, OPERANT; DOPAMINE; FEEDING BEHAVIOR; REWARD;

ANIMALIA; APLYSIA; MOLLUSCA;

EID: 79951580288     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0570-9     Document Type: Review

References (86)

1. JH Byrne DA Baxter DV Buonomano LJ Cleary A Eskin JR Goldsmith E McClendon FA Nazif F Noel KP Scholz 1991 Neural and molecular bases of nonassociative and associative learning in Aplysia Ann N Y Acad Sci 627 124 149 1:CAS:528:DyaK3MXmt1yqt7g%3D 10.1111/j.1749-6632.1991.tb25918.x 1679307
2. DL Glanzman 2006 The cellular mechanisms of learning in Aplysia: of blind men and elephants Biol Bull 210 271 279 10.2307/4134563 16801500
3. RD Hawkins ER Kandel CH Bailey 2006 Molecular mechanisms of memory storage in Aplysia Biol Bull 210 174 191 1:CAS:528:DC%2BD28XnsVahu7c%3D 10.2307/4134556 16801493
4. Reynolds GS (1975) A primer of operant conditioning, 2nd edn. Scott Foresman, Glenview
5. Thorndike EL (1911) Animal intelligence: experimental studies. Macmillan, New York
6. Skinner BF (1938) The behavior of organisms: an experimental analysis. Appleton-Century-Crofts, New York
7. DG Cook TJ Carew 1986 Operant conditioning of head-waving in Aplysia Proc Natl Acad Sci USA 83 1120 1124 1:STN:280:DyaL287kvFahtQ%3D%3D 10.1073/pnas.83.4.1120 3456565
8. AJ Susswein M Schwarz E Feldman 1986 Learned changes of feeding behavior in Aplysia in response to edible and inedible foods J Neurosci 6 1513 1527 1:STN:280:DyaL283is1CqsA%3D%3D 3711992 (Pubitemid 16078037)
9. BF Skinner 1981 Selection by consequences Science 213 501 504 1:STN:280:DyaL3M3isFymsA%3D%3D 10.1126/science.7244649 7244649
10. B Brembs 2003 Operant conditioning in invertebrates Curr Opin Neurobiol 13 710 717 1:CAS:528:DC%2BD3sXps1Oqurc%3D 10.1016/j.conb.2003.10.002 14662373 (Pubitemid 37518459)
11. BJ Everitt TW Robbins 2005 Neural systems of reinforcement for drug addiction: from actions to habits to compulsion Nat Neurosci 8 1481 1489 1:CAS:528:DC%2BD2MXhtFCrurbI 10.1038/nn1579 16251991 (Pubitemid 41573659)
12. RK Pitman 1989 Animal models of compulsive behavior Biol Psychiatry 26 189 198 1:STN:280:DyaL1M3osleqsw%3D%3D 10.1016/0006-3223(89)90022-X 2660914 (Pubitemid 19151122)
13. RN Cardinal BJ Everitt 2004 Neural and psychological mechanisms underlying appetitive learning: links to drug addiction Curr Opin Neurobiol 14 156 162 1:CAS:528:DC%2BD2cXjtV2nu78%3D 10.1016/j.conb.2004.03.004 15082319 (Pubitemid 38479931)
14. AE Kelley 2004 Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning Neurosci Biobehav Rev 27 765 776 10.1016/j.neubiorev.2003.11.015 15019426 (Pubitemid 38202248)
15. BW Balleine 2005 Neural bases of food-seeking: affect, arousal and reward in corticostriatolimbic circuits Physiol Behav 86 717 730 1:CAS:528: DC%2BD2MXht1OltrfK 10.1016/j.physbeh.2005.08.061 16257019 (Pubitemid 41741866)
16. D Belin S Jonkman A Dickinson TW Robbins BJ Everitt 2009 Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction Behav Brain Res 199 89 102 10.1016/j.bbr.2008.09.027 18950658
17. BW Balleine MR Delgado O Hikosaka 2007 The role of the dorsal striatum in reward and decision-making J Neurosci 27 8161 8165 1:CAS:528: DC%2BD2sXpsVGnsLg%3D 10.1523/JNEUROSCI.1554-07.2007 17670959 (Pubitemid 47219597)
18. G Hoyle 1980 Learning, using natural reinforcement, in insect preparations that permit cellular neuronal analysis J Neurobiol 11 323 354 1:STN:280:DyaL3c3ltV2rsw%3D%3D 10.1002/neu.480110402 7400811 (Pubitemid 10063249)
19. G Wustmann K Rein R Wolf M Heisenberg 1996 A new paradigm for operant conditioning of Drosophila melanogaster J Comp Physiol A 179 429 436 1:STN:280:DyaK28znvFGjtg%3D%3D 10.1007/BF00194996 8785009 (Pubitemid 26350827)
20. GE Spencer NI Syed K Lukowiak 1999 Neural changes after operant conditioning of the aerial respiratory behavior in Lymnaea stagnalis J Neurosci 19 1836 1843 1:CAS:528:DyaK1MXhtlGisrw%3D 10024367 (Pubitemid 29094199)
21. D Gardner 1977 Interconnections of identified multiaction interneurons in buccal ganglia of Aplysia J Neurophysiol 40 349 361 1:STN:280: DyaE2s7ktlWjtw%3D%3D 845626 (Pubitemid 8073925)
22. AJ Susswein JH Byrne 1988 Identification and characterization of neurons initiating patterned neural activity in the buccal ganglia of Aplysia J Neurosci 8 2049 2061 1:STN:280:DyaL1c3lvVKjtg%3D%3D 3385489
23. MR Plummer MD Kirk 1990 Premotor neurons B51 and B52 in the buccal ganglia of Aplysia californica: synaptic connections, effect on ongoing motor rhythms, and peptide modulation J Neurophysiol 63 539 558 1:STN:280: DyaK3c3ivFyqug%3D%3D 2329360 (Pubitemid 20115483)
24. I Hurwitz AJ Susswein 1996 B64, a newly identified central pattern generator element producing a phase switch from protraction to retraction in buccal motor programs of Aplysia californica J Neurophysiol 75 1327 1344 1:STN:280:DyaK283otlOmtw%3D%3D 8727381 (Pubitemid 26114048)
25. I Hurwitz I Kupfermann AJ Susswein 1997 Different roles of neurons B63 and B34 that are active during the protraction phase of the buccal motor programs in Aplysia californica J Neurophysiol 78 1305 1319 1:STN:280: DyaK2svlsVentQ%3D%3D 9310422 (Pubitemid 27400673)
26. EA Kabotyanski DA Baxter JH Byrne 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 1:CAS:528:DyaK1cXhsVGruro%3D 9463425 (Pubitemid 28095881)
27. J Jing KR Weiss 2002 Interneuronal basis of the generation of related but distinct motor programs in Aplysia: implications for current neuronal models of vertebrate interlimb coordination J Neurosci 22 6228 6238 1:CAS:528: DC%2BD38XlsFOjt70%3D 12122081 (Pubitemid 35387663)
28. J Jing EC Cropper I Hurwitz KR Weiss 2004 The construction of movement with behavior-specific and behavior-independent modules J Neurosci 24 6315 6325 1:CAS:528:DC%2BD2cXmtFersLc%3D 10.1523/JNEUROSCI.0965-04.2004 15254087 (Pubitemid 38944222)
29. CJH Elliott AJ Susswein 2002 Comparative neuroethology of feeding control in molluscs J Exp Biol 205 877 896 1:STN:280:DC%2BD387osVCrsA%3D%3D 11916985 (Pubitemid 34861226)
30. I Kupfermann 1974 Feeding behavior in Aplysia: a simple system for the study of motivation Behav Biol 10 1 26 1:STN:280:DyaE2c7htFShsQ%3D%3D 10.1016/S0091-6773(74)91644-7 4815142
31. R Nargeot C Petrissans J Simmers 2007 Behavioral and in vitro correlates of compulsive-like food-seeking induced by operant conditioning in Aplysia J Neurosci 27 8059 8070 1:CAS:528:DC%2BD2sXoslSjsbc%3D 10.1523/JNEUROSCI.1950-07. 2007 17652597 (Pubitemid 47173319)
32. D Botzer S Markovich AJ Susswein 1998 Multiple memory processes following training that a food in inedible in Aplysia Learn Mem 5 204 219 1:STN:280:DyaK1Mzot1Wlug%3D%3D 10454365 (Pubitemid 29108880)
33. CM Alberini M Ghirardi R Metz ER Kandel 1994 C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia Cell 76 1099 1114 1:CAS:528:DyaK2cXktlWns7o%3D 10.1016/0092-8674(94)90386-7 8137425 (Pubitemid 24106389)
34. SM Taubenfeld MH Milekic B Monti CM Alberini 2001 The consolidation of new but not reactivated memory requires hippocampal C/EBPβ Nat Neurosci 4 813 818 1:CAS:528:DC%2BD3MXlslSjsLs%3D 10.1038/90520 11477427 (Pubitemid 32702513)
35. D Levitan LC Lyons A Perelman CL Green B Motro A Eskin AJ Susswein 2008 Training with inedible food in Aplysia causes expression of C/EBP in the buccal but not cerebral ganglion Learn Mem 15 412 416 1:CAS:528:DC%2BD1cXotFGnsL4%3D 10.1101/lm.970408 18509115 (Pubitemid 351786969)
36. B Brembs FD Lorenzetti FD Reyes DA Baxter JH Byrne 2002 Operant reward learning in Aplysia: neuronal correlates and mechanisms Science 296 1706 1709 1:CAS:528:DC%2BD38XktlCgtb4%3D 10.1126/science.1069434 12040200 (Pubitemid 34579173)
37. HA Lechner DA Baxter JH Byrne 2000 Classical conditioning of feeding in Aplysia: I. Behavioral Analysis J Neurosci 20 3369 3376 1:CAS:528: DC%2BD3cXivFKhtb0%3D 10777799 (Pubitemid 30263152)
38. R Nargeot DA Baxter JH Byrne 1997 Contingent-dependent enhancement of rhythmic motor patterns: an in vitro analog of operant conditioning J Neurosci 17 8093 8105 1:CAS:528:DyaK2sXntVyjtr8%3D 9334385 (Pubitemid 27461034)
39. R Nargeot DA Baxter JH Byrne 1999 In vitro analog of operant conditioning in Aplysia. I. Contingent reinforcement modifies the functional dynamics of an identified neuron J Neurosci 19 2247 2260 1:CAS:528:DyaK1MXhslKltbk%3D 10066276 (Pubitemid 29133401)
40. R Nargeot DA Baxter JH Byrne 1999 In vitro analogue 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 1:CAS:528:DyaK1MXhslKlur0%3D 10066277 (Pubitemid 29133402)
41. B Brembs DA Baxter JH Byrne 2004 Extending in vitro conditioning in Aplysia to analyze operant and classical processes in the same preparation Learn Mem 11 412 420 10.1101/lm.74404 15254218 (Pubitemid 39079700)
42. HA Lechner DA Baxter JH Byrne 2000 Classical conditioning of feeding in Aplysia: II. Neurophysiological correlates J Neurosci 20 3377 3386 1:CAS:528:DC%2BD3cXivFKhtbo%3D 10777800 (Pubitemid 30263153)
43. FD Lorenzetti R Mozzachiodi DA Baxter JH Byrne 2006 Classical and operant conditioning differentially modify the intrinsic properties of an identified neuron Nat Neurosci 9 17 19 1:CAS:528:DC%2BD2MXhtlCms7rJ 10.1038/nn1593 16311590 (Pubitemid 43011902)
44. FD Lorenzetti DA Baxter JH Byrne 2008 Molecular mechanisms underlying a cellular analog of operant reward learning Neuron 59 815 828 1:CAS:528:DC%2BD1cXhtFKhtbbO 10.1016/j.neuron.2008.07.019 18786364
45. R Mozzachiodi FD Lorenzetti DA Baxter JH Byrne 2008 Changes in neuronal excitability serve as a mechanism of long-term memory for operant conditioning Nat Neurosci 11 1146 1148 1:CAS:528:DC%2BD1cXhtFKhsLzJ 10.1038/nn.2184 18776897
46. DW Morton HJ Chiel 1993 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 1:STN:280:DyaK3s7osl2isw%3D%3D 10.1007/BF00214712 8445578
47. KL Briggman HDI Abarbanel WB Kristan 2005 Optical imaging of neuronal populations during decision-making Science 307 896 901 1:CAS:528: DC%2BD2MXhtFWnu7c%3D 10.1126/science.1103736 15705844 (Pubitemid 40229220)
48. WB Kristan 2008 Neuronal decision-making circuits Curr Biol 18 R928 R932 1:CAS:528:DC%2BD1cXht1entLzK 10.1016/j.cub.2008.07.081 18957243
49. JD Schall 2005 Decision making Curr Biol 15 R9 R11 1:CAS:528: DC%2BD2MXkvFCmsQ%3D%3D 10.1016/j.cub.2004.12.009 15649356
50. R Nargeot DA Baxter GW Patterson JH Byrne 1999 Dopaminergic synapses mediate neuronal changes in an analogue of operant conditioning J Neurophysiol 81 1983 1987 1:CAS:528:DyaK1MXivV2js78%3D 10200235 (Pubitemid 29262531)
51. R Mozzachiodi JH Byrne 2010 More than synaptic plasticity: role of nonsynaptic plasticity in learning and memory Trends Neurosci 33 17 26 1:CAS:528:DC%2BC3cXjtl2qsA%3D%3D 10.1016/j.tins.2009.10.001 19889466
52. M Schwarz AJ Susswein 1986 Identification of the neural pathway for reinforcement of feeding when Aplysia learn that food is inedible J Neurosci 6 1528 1536 1:STN:280:DyaL283is1CqsQ%3D%3D 3711993 (Pubitemid 16078038)
53. CC Horn Y Zhurov IV Orekhova A Proekt I Kupfermann KR Weiss V Brezina 2004 Cycle-to-cycle variability of neuromuscular activity in Aplysia feeding behavior J Neurophysiol 92 157 180 10.1152/jn.01190.2003 14985412 (Pubitemid 38802241)
54. FD Reyes R Mozzachiodi DA Baxter JH Byrne 2005 Reinforcement in an in vitro analog of appetitive classical conditioning of feeding behavior in Aplysia: blockade by a dopamine antagonist Learn Mem 12 216 220 10.1101/lm.92905 15930499 (Pubitemid 40958329)
55. R Nargeot C Cornet J Simmers 2008 Dopaminergic modulation of oscillatory membrane properties of buccal motor-pattern initiating neurons and their electrical coupling in Aplysia FENS Abstr 4 021.13
56. BW Balleine M Liljeholm SB Ostlund 2009 The integrative function of the basal ganglia in instrumental conditioning Behav Brain Res 199 43 52 10.1016/j.bbr.2008.10.034 19027797
57. G Kemenes K Staras PR Benjamin 2001 Multiple types of control by identified interneurons in a sensory-activated rhythmic motor pattern J Neurosci 21 2903 2911 1:CAS:528:DC%2BD3MXjtVWrs7Y%3D 11306642 (Pubitemid 32298231)
58. R Nargeot M Le Bon-Jego J Simmers 2009 Cellular and network mechanisms of operant learning-induced compulsive behaviour in Aplysia Curr Biol 19 975 984 1:CAS:528:DC%2BD1MXnsFOqtb0%3D 10.1016/j.cub.2009.05.030 19500988
59. TR Chay 1996 Electrical bursting and luminal calcium oscillation in excitable cell models Biol Cybern 75 419 431 1:STN:280:DyaK2s7jslyhtA%3D%3D 10.1007/s004220050307 8983163 (Pubitemid 126676901)
60. AI Selverston MI Rabinovich HDI Abarbanel R Elson A Szücs RD Pinto R Huerta P Varona 2000 Reliable circuits from irregular neurons: a dynamical approach to understanding central pattern generators J Physiol (Paris) 94 357 374 1:STN:280:DC%2BD3M3hsVegsQ%3D%3D 10.1016/S0928-4257(00)01101-3 (Pubitemid 32110920)
61. P Varona JJ Torres R Huerta HDI Abarbanel MI Rabinovich 2001 Regularization mechanisms of spiking-bursting neurons Neural Netw 14 865 875 1:STN:280:DC%2BD3MrmsVGisQ%3D%3D 10.1016/S0893-6080(01)00046-6 11665777 (Pubitemid 33035880)
62. 3 Biol Cybern 82 517 527 1:STN:280: DC%2BD3cvmvFCltg%3D%3D 10.1007/s004220050604 10879435
63. TJ Lewis J Rinzel 2000 Self-organized synchronous oscillations in a network of excitable cells coupled by gap junctions Network 11 299 320 1:STN:280:DC%2BD3M7it1WisA%3D%3D 10.1088/0954-898X/11/4/304 11128169
64. DG Placantonakis AA Bukovsky SA Aicher H-P Kiem JP Welsh 2006 Continuous electrical oscillations emerge from a coupled network: a study of the inferior olive using lentiviral knockdown of connexin36 J Neurosci 26 5008 5016 1:CAS:528:DC%2BD28Xlt1Cjur8%3D 10.1523/JNEUROSCI.0146-06.2006 16687492 (Pubitemid 44315282)
65. EM Lasater 1987 Retinal horizontal cell gap junctional conductance is modulated by dopamine through a cyclic AMP-dependent protein kinase Proc Natl Acad Sci USA 84 7319 7323 1:CAS:528:DyaL2sXmtFagtb8%3D 10.1073/pnas.84.20.7319 2823257
66. XD Yang H Korn DS Faber 1990 Long-term potentiation of electrotonic coupling at mixed synapses Nature 348 542 545 1:STN:280:DyaK3M%2FmtF2juw%3D%3D 10.1038/348542a0 2174130 (Pubitemid 120015105)
67. BR Johnson JH Peck RM Harris-Warrick 1993 Amine modulation of electrical coupling in the pyloric network of the lobster stomatogastric ganglion J Comp Physiol A 172 715 732 1:STN:280:DyaK3szltlCguw%3D%3D 10.1007/BF00195397 8350285
68. L Kokarovtseva T Jaciw-Zurakiwsky R Mendizabal Arbocco MV Frantseva JL Perez Velazquez 2009 Excitability and gap junction-mediated mechanisms in nucleus accumbens regulate self-stimulation reward in rats Neuroscience 159 1257 1263 1:CAS:528:DC%2BD1MXktFeksLg%3D 10.1016/j.neuroscience.2009.01.065 19409225
69. W Schultz 1997 Dopamine neurons and their role in reward mechanisms Curr Opin Neurobiol 7 191 197 1:CAS:528:DyaK2sXjsVOrtLo%3D 10.1016/S0959-4388(97) 80007-4 9142754 (Pubitemid 27219855)
70. W Schultz 2010 Dopamine signals for reward value and risk: basic and recent data Behav Brain Funct 23 6 24
71. RA Wise PP Rompre 1989 Brain dopamine and reward Annu Rev Psychol 40 191 225 1:STN:280:DyaL1M7pt1anuw%3D%3D 10.1146/annurev.ps.40.020189.001203 2648975
72. RA Wise 2004 Dopamine and food reward: back to the elements Am J Physiol Regul Integr Comp Physiol 286 R13 1:CAS:528:DC%2BD2cXot1SgtQ%3D%3D 14660469
73. G Di Chiara V Bassareo 2007 Reward system and addiction: what dopamine does and doesn't do Curr Opin Pharmacol 7 69 76 1:CAS:528:DC%2BD2sXntlGhsw%3D%3D 10.1016/j.coph.2006.11.003 17174602 (Pubitemid 46238042)
74. JW Dalley BJ Everitt 2009 Dopamine receptors in the learning, memory and drug reward circuitry Semin Cell Dev Biol 20 403 410 1:CAS:528: DC%2BD1MXnslyrtLc%3D 10.1016/j.semcdb.2009.01.002 19560045
75. S Fulton 2010 Appetite and reward Front Neuroendocrinol 31 85 103 10.1016/j.yfrne.2009.10.003 19822167
76. J Olds P Milner 1954 Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain J Comp Physiol Psychol 47 419 427 1:STN:280:DyaG2M%2FksFahtQ%3D%3D 10.1037/h0058775 13233369
77. M Le Moal H Simon 1991 Mesocorticolimbic dopaminergic network: Functional and regulatory roles Physiol Rev 71 155 234 1:STN:280:DyaK3M%2FpsFClug%3D%3D 1986388
78. A Ettenberger 1989 Dopamine, neuroleptics and reinforced behavior Neurosci Biobehav Rev 13 105 111 10.1016/S0149-7634(89)80018-1
79. SL Smith-Roe AE Kelley 2000 Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning J Neurosci 20 7737 7742 1:CAS:528:DC%2BD3cXns1eitr4%3D 11027236
80. Z Liu BJ Richmond EA Murray RC Saunders S Steenrod BK Stubblefield DM Montague EI Ginns 2004 DNA targeting of rhinal cortex D2 receptor protein reversibly blocks learning of cues that predict reward Proc Natl Acad Sci USA 101 12336 12341 1:CAS:528:DC%2BD2cXntFektLs%3D 10.1073/pnas.0403639101 15302926 (Pubitemid 39145444)
81. JP Fadok TMK Dickerson RD Palmiter 2009 Dopamine is necessary for cue-dependent fear conditioning J Neurosci 29 11089 11097 1:CAS:528: DC%2BD1MXhtFOhu73J 10.1523/JNEUROSCI.1616-09.2009 19741115
82. C Martínez-Rubio GE Serrano MW Miller 2009 Localization of biogenic amines in the foregut of Aplysia californica: catecholaminergic and serotonergic innervation J Comp Neurol 514 329 342 10.1002/cne.21991 19330814
83. P Ascher 1972 Inhibitory and excitatory effects of dopamine on Aplysia neurons J Physiol (London) 225 173 209 1:CAS:528:DyaE38XltV2gsLw%3D
84. JW Swann CN Sinback DO Carpenter 1978 Evidence for identified dopamine motor neurons to the gill of Aplysia Neurosci Lett 10 275 280 1:CAS:528:DyaE1MXotlynuw%3D%3D 10.1016/0304-3940(78)90239-2 19605293 (Pubitemid 9087866)
85. NJ Wright RJ Walker 1984 The possible site of action of 5-hydroxytryptamine, 6-hydroxytryptamine, tryptamine and dopamine on identified neurons in the central nervous system of the snail, Helix aspersa Comp Biochem Physiol C 78 217 225 1:STN:280:DyaL2c3mtVCqsA%3D%3D 10.1016/0742-8413(84)90073-2 6146474 (Pubitemid 14112558)
86. T Teyke SC Rosen KR Weiss I Kupfermann 1993 Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry of Aplysia Brain Res 630 26 237 10.1016/0006-8993(93)90661-6 (Pubitemid 23342845)