Spontaneous decisions and operant conditioning in fruit flies

Behavioural Processes

Volumn 87, Issue 1, 2011, Pages 157-164

  Brembs, Björn ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Drosophila; Insect; Learning; Memory; Multiple memory systems; Operant; Self learning; World learning

Indexed keywords

BEHAVIORAL ECOLOGY; BRAIN; DATA SET; DECISION MAKING; FLY; FRUIT; INHIBITION; MEMORY; MUSHROOM; NEUROLOGY; RESEARCH WORK;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DROSOPHILA; INSTRUMENTAL CONDITIONING; LEARNING; MEMORY; NEUROPIL; NONHUMAN;

ANIMALS; CONDITIONING, CLASSICAL; CONDITIONING, OPERANT; DECISION MAKING; DROSOPHILA; LEARNING; MUSHROOM BODIES;

BASIDIOMYCOTA; HEXAPODA;

EID: 79954981034     PISSN: 03766357     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.beproc.2011.02.005     Document Type: Article

References (80)

1. Alkon D.L. Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science 1984, 226:1037-1045.
2. Antonov I., Antonova I., Kandel, Eric R., Hawkins R.D. The contribution of activity-dependent synaptic plasticity to classical conditioning. J. Neurosci. 2001, 21:6413-6422.
3. Baden-Powell R. Scouting for Boys. C 1908, Arthur Pearson Ltd, London.
4. Balleine B.W., Ostlund S.B. Still at the choice-point: action selection and initiation in instrumental conditioning. Ann. N.Y. Acad. Sci. 2007, 1104:147-171.
5. Balleine B.W., O'Doherty J.P. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 2010, 35:48-69.
6. Brembs, B. 2008, Operant learning of Drosophila at the torque meter. J. Vis. Exp. 16, http://www.jove.com/details.stp%3Fid=731%20doi%3A10.3791/731.
7. Brembs B. Mushroom bodies regulate habit formation in Drosophila. Curr. Biol. 2009, 19:1351-1355.
8. Brembs B. The importance of being active. J. Neurogen. 2009, 23:120-126.
9. Brembs B. Towards a scientific concept of free will as a biological trait: spontaneous actions and decision-making in invertebrates. Proc. R. Soc. B. 2010, 278(1707):930-939.
10. Brembs B., Heisenberg M. Conditioning with compound stimuli in Drosophila melanogaster in the flight simulator. J. Exp. Biol. 2001, 204:2849-2859.
11. Brembs B., Heisenberg M. The operant and the classical in conditioned orientation of Drosophila melanogaster at the flight simulator. Learn. Mem. 2000, 7:104-115.
12. Brembs B., Hempel De Ibarra N. Different parameters support generalization and discrimination learning in Drosophila at the flight simulator. Learn. Mem. 2006, 13:629-637.
13. Brembs B., Lorenzetti F.D., Reyes F.D., Baxter D.A., Byrne J.H. Operant reward learning in Aplysia: neuronal correlates and mechanisms. Science 2002, 296:1706-1709.
14. Brembs, B., Pauly, D., Schade, R., Mendoza, E., Pflüger, H.-J., Rybak, J., Scharff, C., Zars, Troy. 2010. The Drosophila FoxP gene is necessary for operant self-learning: Implications for the evolutionary origins of language. In Soc. Neurosci., p. 704.7, San Diego, Ca., USA.
15. Brembs B., Plendl W. Double dissociation of pkc and ac manipulations on operant and classical learning in Drosophila. Curr. Biol. 2008, 18:1168-1171.
16. Brembs B., Wiener J. Context and occasion setting in drosophila visual learning. Learn. Mem. 2006, 13:618-628.
17. Byrne J.H., Kandel E.R. Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 1996, 16:425-435.
18. Colomb J., Brembs B. The biology of psychology: "simple" conditioning?. Comm. Int. Biol. 2010, 3:142-145.
19. Colomb J., Mendoza E., Pauly D., Raja S., Brembs B. The what and where of operant self-learning mechanisms in Drosophila. 9th International Congress of Neuroethology 2010, Salamanca, Spain, p. P279.
20. Crow T.J., Alkon D.L. Associative behavioral modification in Hermissenda: cellular correlates. Science 1980, 209:412-414.
21. Disterhoft J.F., Coulter D.A., Alkon D.L. Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc. Nat. Acad. Sci. 1986, 83:2733-2737.
22. Donahoe J.W. Selection networks: simulation of plasticity through reinforcement learning. Advances in Psychology 1997, 336-357. Elsevier Science B V. V. Packard Dorsel (Ed.).
23. Donahoe J.W., Burgos J.E., Palmer D.C. A selectionist approach to reinforcement. J. Exp. Anal. Behav. 1993, 60:17-40.
24. Drier E.A., Tello M.K., Cowan M., Wu P., Blace N., Sacktor, Todd Charlton, Yin J.C.P. Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster. Nat. Neurosci. 2002, 5:316-324.
25. Ernst R., Heisenberg M. The memory template in Drosophila pattern vision at the flight simulator. Vis. Res. 1999, 39:3920-3933.
26. Farley J., Alkon D.L. Cellular mechanisms of learning, memory, and information storage. Ann. Rev. Psych. 1985, 36:419-494.
27. Fisher, Simon E., Scharff C. FOXP2 as a molecular window into speech and language. Trends Genet. 2009, 25:166-177.
28. Gormezano I., Tait R.W. The Pavlovian analysis of instrumental conditioning. Integr. Psych. Behav. Sci. 1976, 11:37-55.
29. Guthrie E.R. The Psychology of Learning 1952, Harper, New York.
30. Götz K.G. Optomotorische Untersuchung des visuellen systems einiger Augenmutanten der Fruchtfliege Drosophila 1964, Kybernetik2, pp. 77-92.
31. Haesler S., Rochefort C., Georgi B., Licznerski P., Osten P., Scharff C. Incomplete and inaccurate vocal imitation after knockdown of foxp2 in songbird basal ganglia nucleus area X. PLoS Biol. 2007, 5:12.
32. Heisenberg M. Voluntariness (Willkürfähigkeit) and the general organization of behavior. L. Sci. Res. Rep. 1994, 55:147-156.
33. Heisenberg M., Wolf R. Vision in Drosophila. Genetics of Microbehavior 1984, Springer, Berlin, Heidelberg, New York, Tokio.
34. Heisenberg M., Wolf R., Brembs B. Flexibility in a single behavioral variable of Drosophila. Learn. Mem. 2001, 8:1-10.
35. Heisenberg M. Initiale Aktivität und Willkürverhalten bei Tieren. Naturwissenschaften 1983, 70:70-78.
36. Hellige J.B., Grant D.A. Eyelid conditioning performance when the mode of reinforcement is changed from classical to instrumental avoidance and vice versa. J. Exp. Psych. 1974, 102:710-719.
37. Jaffard R., Jeantet Y. Posttraining changes in excitability of the commissural path-CA1 pyramidal cell synapse in the hippocampus of mice. Brain Res. 1981, 220. 167-172.
38. Jones N.G., Kemenes I., Kemenes G., Benjamin P.R. A persistent cellular change in a single modulatory neuron contributes to associative long-term memory. Curr. Biol. 2003, 13:1064-1069.
39. Kemenes I., Straub V.A., Nikitin E.S., Staras K., O'Shea M., Kemenes G., Benjamin P.R. Role of delayed nonsynaptic neuronal plasticity in long-term associative memory. Curr. Biol. 2006, 16:1269-1279.
40. Kokarovtseva L., Jaciw-Zurakiwsky T., MendizabalArbocco R., Frantseva M.V., Perez Velazquez J.L. Excitability and gap junction-mediated mechanisms in nucleus accumbens regulate self-stimulation reward in rats. Neuroscience 2009, 159:1257-1263.
41. Konorski J., Miller S. On two types of conditioned reflex. J. Gen. Psych. 1937, 16:264-272.
42. Konorski J., Miller S. Further remarks on two types of conditioned reflex. J. Gen. Psych. 1937, 17:405-407.
43. Kornell and Terrace, Kornell, N., Terrace, H.S. 2007, The generation effect in monkeys. Psych. Sci. 18, 682-685. http://www.blackwell-synergy.com/doi/abs/10.1111/j.1467-9280.2007.01959.x.
44. Lai C.S., Fisher S.E., Hurst J.A., Vargha-Khadem F., Monaco A.P. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 2001, 413:519-523.
45. Liu G., Seiler H., Wen A., Zars T., Ito K., Wolf R., Heisenberg M., Liu L. Distinct memory traces for two visual features in the Drosophila brain. Nature 2006, 439:551-556.
46. Lorenzetti F.D., Mozzachiodi R., Baxter D.A., Byrne J.H. Classical and operant conditioning differentially modify the intrinsic properties of an identified neuron. Nat. Neurosci. 2006, 9:17-29.
47. Lorenzetti F.D., Baxter D.A., Byrne J.H. Molecular mechanisms underlying a cellular analog of operant reward learning. Neuron 2008, 59:815-828.
48. Maye A., Hsieh C.-H, Sugihara G., Brembs B. Order in spontaneous behavior. PLoS ONE 2007, 2. e443.
49. Moyer J.R., Thompson L.T., Disterhoft J.F. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J. Neurosci. 1996, 16:5536-5546.
50. Mozzachiodi R., Byrne J.H. More than synaptic plasticity: role of nonsynaptic plasticity in learning and memory. Trends Neurosci. 2010, 33:17-26.
51. Nargeot R. Correlation between activity in neuron B52 and two features of fictive feeding in Aplysia. Neurosci. Lett. 2002, 328:85-88.
52. Nargeot R., Baxter D.A., Byrne J.H. Contingent-dependent enhancement of rhythmic motor patterns: an in vitro analog of operant conditioning. J. Neurosci. 1997, 17:8093-8105.
53. Nargeot R., Baxter D.A., Byrne J.H. 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. 1999, 19:2261-2272.
54. Nargeot R., Baxter D.A., Patterson G.W., Byrne J.H. Dopaminergic synapses mediate neuronal changes in an analogue of operant conditioning. J. Neurophys 1999, 81:1983-1987.
55. Nargeot R., Baxter D.A., Byrne J.H. In vitro analog of operant conditioning in Aplysia I. Contingent reinforcement modifies the functional dynamics of an identified neuron. J. Neurosci. 1999, 19:2247-2260.
56. Nargeot R., Baxter D.A., Byrne J.H. 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. 1999, 19:2261-2272.
57. Nargeot R., Le Bon-Jego M., Simmers J. Cellular and network mechanisms of operant learning-induced compulsive behavior in Aplysia. Curr. Biol. 2009, 19:975-984.
58. Nargeot R., Petrissans C., Simmers J. Behavioral and in vitro correlates of compulsive-like food seeking induced by operant conditioning in Aplysia. J. Neurosci. 2007, 27:8059-8070.
59. Nargeot R., Simmers J. Neural mechanisms of operant conditioning and learning-induced behavioral plasticity in Aplysia. Cell. Mol. Life Sci. 2010, 10.1007/s00018-010r-r0570-9.
60. Olds J.L., Alkon D.L. A role for protein kinase C in associative learning. New Biol. 1991, 3:27-35.
61. Olds J.L., Anderson M.L., McPhie D.L., Staten L.D., Alkon D.L. Imaging of memory-specific changes in the distribution of protein kinase C in the hippocampus. Science 1989, 245:866-869.
62. Plummer M.R., Kirk M.D. Premotor neurons B51 and B52 in the buccal ganglia of Aplysia californica: synaptic connections, effects on ongoing motor rhythms, and peptide modulation. J. Neurophys. 1990, 63:539-558.
63. Rescorla R.A., Solomon R.L. Two-process learning theory: Relationships between Pavlovian conditioning and instrumental learning. Psych. Rev. 1967, 74:151-182.
64. Santos M.E., Athanasiadis A., Leitão A.B., Dupasquier L., Sucena E. Alternative splicing and gene duplication in the evolution of the FoxP gene sub-family. Mol. Biol. Evol. 2010, 28:237-247.
65. Sheffield F.D. Relation of classical conditioning and instrumental learning. Classical Conditioning 1965, 302-322. Appleton-Century-Crofts, New York. W.F. Prokasy (Ed.).
66. Shema R., Hazvi S., Sacktor, Todd C., Dudai Y. Boundary conditions for the maintenance of memory by PKMzeta in neocortex. Learn. Mem. 2009, 16:122-128.
67. Skinner B.F. Two types of conditioned reflex and a pseudo type. J. Gen. Psych. 1935, 12:66-77.
68. Skinner B.F. Two types of conditioned reflex: a reply to Konorski and Miller. J. Gen. Psych. 1937, 16:272-279.
69. Slamecka N.J., Graf P. Generation Effect - Delineation of a Phenomenon. J. Exp. Psych.: Hum. Learn. Mem. 1978, 4:592-604.
70. Sossin W.S. Isoform specificity of protein kinase Cs in synaptic plasticity. Learn. Mem. 2007, 14:236-246.
71. Tang S.M., Wolf R., Xu S.P., Heisenberg M. Visual pattern recognition in Drosophila is invariant for retinal position. Science 2004, 305:1020-1022.
72. Thorndike E.L. Animal Intelligence. An Experimental Study of the Associative Processes in Animals 1898, Macmillan, New York.
73. Trapold M.A., Overmier J.B. The second learning process in instrumental conditioning. In Classical conditioning II. Current Research and Theory 1972, 427-452. Appleton-Century-Crofts, New York. A.H. Black, W.F. Prokasy (Eds.).
74. Trapold M.A., Winokur S. Transfer from classical conditioning and extinction to acquisition, extinction, and stimulus generalization of a positively reinforced instrumental response. J. Exp. Psych. 1967, 73:517-525.
75. Villareal G., Li Q., Cai D., Fink A.E., Lim T., Bougie J.K., Sossin W.S., Glanzman D.L. Role of protein kinase C in the induction and maintenance of serotonin-dependent enhancement of the glutamate response in isolated siphon motor neurons of Aplysia californica. J. Neurosci. 2009, 29:5100-5107.
76. Wolf R., Heisenberg M. Visual orientation in motion-blind flies is an operant behavior. Nature 1986, 323:154-156.
77. Wolf R., Heisenberg M. Visual space from visual motion: turn integration in tethered flying Drosophila. Learn. Mem. 1997, 4:318-327.
78. Wolf R., Heisenberg M. Basic organization of operant behavior as revealed in Drosophila flight orientation. J. Comp. Physiol. 1991, A169:699-705.
79. Wolf R., Voss A., Hein S., Heisenberg M. Can a fly ride a bicycle? Discussion on Natural and Artificial Low-Level Seeing Systems. Phil. Trans. Roy. Soc. B: Biol. Sci. 1992, 337:261-269.
80. Zhao Y.L., Leal K., Abi-Farah C., Martin K.C., Sossin W.S., Klein M. Isoform specificity of PKC translocation in living Aplysia sensory neurons and a role for Ca2+ -dependent PKC APL I in the induction of intermediate-term facilitation. J. Neurosci. 2006, 26:8847-8856.