Habituation, sensitization, and Pavlovian conditioning

Frontiers in Integrative Neuroscience

Volumn 8, Issue FEB, 2014, Pages

  Çevik, Münire Özlem ^a  

^a TOBB UNIVERSITY OF ECONOMICS AND TECHNOLOGY   (Turkey)

Author keywords

Dopamine; Drosophila melanogaster; Habituation; Mushroom bodies; Olfactory conditioning; Proboscis extension response

Indexed keywords

EID: 84894036377     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2014.00013     Document Type: Article

References (63)

1. Acevedo, S. F., Froudarakis, E. I., Kanellopoulos, A., and Skoulakis, E. M. C. (2007). Protection from premature habituation requires functional mushroom bodies in Drosophila. Learn. Mem. 14, 376-384. doi: 10.1101/lm.566007
2. Agroff, C. E., Albrecht, P., Irving, G., and Rice, F. (2009). Multimodal analgesia for chronic pain: rationale and future directions. Pain Med. (Suppl 2), S53-S66. doi: 10.1111/j.1526-4637.2009.00669.x
3. Aso, Y., Herb, A., Ogueta, M., Siwanowics, I., Templier, T., Friedrich, A. B., et al. (2012). Three dopamine pathways induce aversive odor memories with different stability. PLoS Genet. 8:e1002768. doi: 10.1371/journal.pgen.1002768
4. Barrionuevo, G., and Brown, T. H. (1983). Associative long term potentiation in hippocampal slices. Proc. Natl. Acad. Sci. U.S.A. 80, 7347-7351. doi: 10.1073/pnas.80.23.7347
5. Bliss, T. V., and Lomo, T. (1973). Long lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356.
6. Burke, C., Huetteroth, W., Owald, D., Perisee, E., Krashes, M. J., Das, G., et al. (2012). Layered reward signaling through octopamine and dopamine in Drosophila. Nature 492, 433-437. doi: 10.1038/nature11614
7. Cevik, M. O., and Erden, A. (2012). The course of habituation of the proboscis extension reflex can be predicted by sucrose responsiveness in Drosophila. PLoS ONE 7:e38963. doi: 10.1371/journal.pone.0039863
8. Chabaud, M. A., Devaud, J. M., Pham-Delègue, M. H., Preat, T., and Kaiser, L. (2006). Olfactory conditioning of proboscis activity in Drosophila melanogaster. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 192, 1335-1348. doi: 10.1007/s00359-006-0160-3
9. Chen, C. C., Wu, J. K., Lin, H. W., Pai, T. P., Fu, T. F., Wu, C. L., et al. (2012). Visualizing long term memory formation in two neurons of the Drosophila brain. Science 335, 678-685. doi: 10.1126/science.1212735
10. Crickmore, V. A., and Vosshall, L. B. (2013). Opposing dopaminergic and GABAergic durations control the duration and persistence of copulation in Drosophila. Cell 155, 881-893. doi: 10.1016/j.cell.2013.09.055
11. Dahanukar, A., Lei, Y. T., Kwon, J. Y., and Carlson, J. R. (2007). Two Gr genes underlie sugar reception in Drosophila. Neuron, 56, 503-516. doi: 10.1016/j.neuron.2007.10.024
12. Davis, M., and Whalen, P. J. (2001). Amygdala: vigilance and emotion. Mol. Psychiatry 6, 13-34. doi: 10.1038/sj.mp.4000812
13. de Araujo, I. E. (2011). Sweet taste signaling and the formation of memories of energy sources. Front. Syst. Neurosci. 5:99. doi: 10.3389/fnsys.2011.00099
14. Dethier, V. (1974). "Sensory input and the inconstant fly," in ExperimentalAnalysis of Insect Behavior, ed L. Barton Browne (New York, NY: Springer Verlag), 1-31. doi: 10.1007/978-3-642-86666-1_3
15. Durlach, P. J. (1989). "Learning and performance in pavlovian conditioning: are failures of contiguity failures of learning or performance?" in Contemporary Learning Theories: Pavlovian Conditioning and the Status of Learning Theory, eds S. B. Klein and R. R. Mowrer (Hillsdale, NJ: Lawrence Erlbaum Associates), 19-69.
16. Edgecomb, R. S. et al. (1987). Regulation of tarsal taste threshold in the blowfly, Phormia regina. J. Exp. Biol. 127, 70-94.
17. Fernandez-Ruiz, J., Miranda, M. I., Bermudez-Rattoni, F., and Drucker-Colm, R. (1993). Effects of catecholaminergic depletion of the amygdala and the insular cortex on the potentiation of odor by taste aversions. Behav. Neural Biol. 60, 189-191. doi: 10.1016/0163-1047(93)90314-8
18. Franklin, S., and Hall, G. (2011). Analysis of US-preexposure effects in appetitive conditioning. J. Exp. Psychol. Anim. Behav. Process. 37, 495-500. doi: 10.1037/a0025484
19. Fujita, M., and Tanimura, T. (2011). Drosophila evaluates and learns the nutritional value of sugars. Curr. Biol. 21, 751-755. doi: 10.1016/j.cub.2011.03.058
20. Gallistel, C. R., and Matzel, L. D. (2013). The neuroscience of learning: beyond the Hebbian synapse. Ann. Rev. Psychol. 64, 169-200. doi: 10.1146/annurev-psych- 113011-143807
21. Garcia, J., and Koelling, R. (1966). Relation of cue to consequence in avoidance learning. Psychon. Sci. 4, 123-124.
22. Gaudry, Q., and Kristan, W. B. Jr. (2012). Decision points: the factors influencing the decision to feed in the medicinal leech. Front. Neurosci. 6:101. doi: 10.3389/fnins.2012.00101
23. Glanzman, D. L. (2009). Habituation in Aplysia: the Cheshire cat of neurobiology. Neurobiol. Learn. Mem. 92, 147-154. doi: 10.1016/j.nlm.2009.03.005
24. Gormezano, I., and Kehoe, E. J. (1981). "Classical conditioning and the law of contiguity," in Advances in Analysis of Behavior: Predictability, Correlation, and Contiguity, eds P. Harzem and M. D. Zeiler (New York, NY: John Wiley & Sons), 1-45.
25. Hall, G. (2001). "Perceptual learning: association and differentiation," in Handbook of Contemporary Learning Theories, eds R. R. Mowrer and B. K. Stephen (Mahwah, NJ: Lawrence Erlbaum Associates), 367-407.
26. Hatfield, T., Graham, P. W., and Gallagher, M. (1992). Taste potentiated odor aversion: a role of the amygdaloid basolateral complex and central nucleus. Behav. Neurosci. 106,286-293. doi: 10.1037/0735-7044.106.2.286
27. Horn, G., and Hinde, R. A. (1970). Short Term Changes in Neural Activity and Behavior. London; New York, NY: Cambridge University Press.
28. Howe, M. W., Tierney, P. L., Sandberg, S. G., Phillips, P. E., and Graybiel, A. M. (2013). Prolonged dopamine signaling in striatum signals proximity and value of distant rewards. Nature 500, 575-579. doi: 10.1038/nature12475
29. Inagaki, H. K., Ben-Tabou de-Leon, S., Wong, A. M., Jagadish, S., Ishimoto, H., Barnea, G., et al. (2012). Visualizing neuromodulation in vivo: TANGO-mapping of dopamine signaling reveals appetite control of sugai sensing. Cell 148, 583-595. doi: 10.1016/j.cell.2011.12.022
30. Kamin, L. J. (1968). Attention-like processes in classical conditioning, in Miam, Symposium on the Prediction of Behavior 1967: Aversive stimulation, ed M. R Jones (Florida, FL: University of Miami Press), 9-31.
31. Kaye, W. H., Wagner, A., Fudge, J. L., and Paulus, M. (2011). Neurocircuitry of eating disorders. Curr. Top. Behav. Neurosci. 6, 37-57. doi: 10.1007/7854_2010_85
32. Keene, A. C., and Waddell, S. (2007). Drosophila olfactory memory: single genes tc complex circuits. Nat. Rev. Neurosci. 8, 341-354. doi: 10.1038/nrn2098
33. Krashes, M. J., DasGupta, S., Vreede, A., White, B., Armstrong, J. D., and Waddell, S. (2009). A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139, 416-427. doi: 10.1016/j.cell.2009.08.035
34. Krashes, M. J., Keene, A. C., Leung, B., Armstrong, J. D., and Waddell, S. (2007). Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53, 103-115. doi: 10.1016/j.neuron.2006.11.021
35. Liu, L., Wolf, R., Ernst, R., and Heisenberg, M. (1999). Context generalization in Drosophilavisual learning requires the mushroom bodies. Nature 400, 753-756 doi: 10.1038/22919
36. Liu, C., Placais, P. Y., Yamagata, N., Pfeiffer, B. D., Yoshinori, A., Friedrich AB. et al. (2012). A subset of dopamine neurons signals reward for odor memory in Drosophila. Nature, 488, 512-517. doi: 10.1038/nature11304
37. LoLordo, V. M., and Randich, A. (1981). "Effects of experience of electric shock upon subsequent conditioning of an emotional response: associative and non- associative accounts, in Predictability, Correlation, Contiguity, eds P. Harzem and M. H. Zeiler (New York, NY: John Wiley & Sons Ltd), 247-285.
38. Malkinson, G., and Spira, M. E. (2013). Release properties of individual presy- naptic boutons expressed during homosynaptic depression and heterosynaptic facilitation of the Aplysia sensorimotor synapse. Front. Cell Neurosci. 7:165. doi: 10.3389/fncel.2013.00165
39. Mao, Z., and Davis, R. (2009). Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiologica heterogeneity. Front. Neural Circuits 3:5. doi: 10.3389/neuro.04.005.2009
40. Marella, S., Mann, K., and Scott, K. (2012). Dopaminergic modulation of sucrose acceptance behavior in Drosophila. Neuron 73, 941-950. doi 10.1016/j.neuron.2011.12.032
41. Mizunami, M., Weibrect, J. M., and Strausfeld, N. J. (1998). Mushroom bodies of the cockroach: Their participation in place memory. J. Comp. Neurol 402, 520-537. doi: 10.1002/(SICI)1096-9861(19981228)402:4<520::AID- CNE6>3.0.C0;2-K
42. Pai, T. P., Chen, C. C., Lin, H. H., Chin, A. L., Lai, J. S., Lee, P. T., et al. (2013). Drosophila ORB protein in two mushroom body output neurons is necessary for long term memory formation. Proc. Natl. Acad. Sci. U.S.A. 110, 7898-7903. doi: 10.1073/pnas.1216336110
43. Pearce, J. M., and Hall, G. (1980). A model for Pavlovian learning: variations in the effectiveness of conditioned but not unconditioned stimuli. Psychol. Rev. 87. 532-552. doi: 10.1037/0033-295X.87.6.532
44. Pitman, J., Huetteroth, W., Burke, C., Krashes, M. J., Lai, S. L., Lee, T. et al. (2011). A pair of inhibitory neurons is required to sustain labile memory in the Drosophila mushroom body. Curr. Biol. 21, 855-861. doi: 10.1016/j.cub.2011.03.069
45. Placais, P. Y., Trannoy, S., Friedrich, A. B., Tanimoto, H., and Preat, T. (2013). Two pairs of mushroom body efferent neurons are required for appetitive long term memory retrieval in Drosophila. Cell Rep. 5, 769-780. doi 10.1016/j.celrep.2013.09.032
46. Reiss, S., and Wagner, A. R. (1972). CS habituation produces a latent inhibition effect but no active conditioned inhibition. Learn. Motiv. 3, 237-245. doi: 10.1016/0023-9690(72)90020-3
47. Rescorla, R. A. (1973). "Second order conditioning: implications for theories of learning, in Contemporary Approaches to Learning and Conditioning, eds F. J. McGuigan and D. Lumsden (New York, NY: Winston), 127-150.
48. Rescorla, R. A., and Holland, P. C. (1988). Behavioral studies of pavlovian conditioning. Ann. Rev. Neurosci. 11, 329-352. doi: 10.1146/annurev.ne.11.030188 001553
49. Rescorla, R. A., and Wagner, A. R. (1972). "A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and non-reinforcement in Classical Conditioning II, eds A. H. Black and W. F. Prokasky (New York, NY: Appleton-Century-Crofts), 64-99.
50. Stewart, J., and Vezina, P. (1988). "Conditioning and behavioral sensitization, in Sensitization in the Nervous System, eds P. W. Kalivas and C. D. Barnes (Caldwell, NJ: The Telford Press), 207-224.
51. Strausfeld, N. J. (2012). Arthropod Brains: Evolution, Functional Elegance and Historical Significance. Cambridge, MA: The Belknap Press of Harvard University Press.
52. Strausfeld, N. J., Sinakevitch, I., and Vilinsky, I. (2003). The mushroom bodies of Drosophila melanogaster: immunocytological and golgi study of kenyon cell organization in the calyces and lobes. Microsc. Res. Tech. 62, 151-169. doi: 10.1002/jemt.10368
53. Timberlake, W. (1994). Behavior systems, associationism and Pavlovian conditioning. Psychon. Bull. Rev. 1, 405-420. doi: 10.3758/BF03210945
54. Tinbergen, N. (1951). TheStudyofInstinct. Oxford: Oxford University Press.
55. Tully, K., Li, Y., Tsvetkov, E., and Bolshakov, V. Y. (2007). Norepinephrine enables the induction of associative long term potentiation at thalamo- amygdala synapses. Proc. Natl. Acad. Sci. U.S.A. 104, 14146-14150. doi: 10.1073/pnas.0704621104
56. Tully, T., and Quinn, W. G. (1985). Classical conditioning and retention in normal and adult Drosophila melanogaster. J. Comp. Physiol. A 157, 263-277. doi: 10.1007/BF01350033
57. van Swinderen, B. (2007). Attention like processes in Drosophila require short term memory genes. Science 315, 1590-1593. doi: 10.1126/science. 1137931
58. Vargo, M., and Hirsch, J. (1982). Central excitation in the fruit fly (Drosophila melanogaster). J. Comp. Physiol. Psychol. 96, 452-459. doi: 10.1037/ h0077899
59. Wittmann, B. C., Schott, B. H., Guderian, S., Frey, J. U., Heinze, H. J., and Düzel, E. (2005). Reward-related fMRI activation of dopaminergic midbrain is associated with enhanced hippocampus dependent long term memory formation. Neuron 45, 459-467. doi: 10.1016/j.neuron.2005.01.010
60. Xia, S., Miyashita, T., Fu, T. F., Lin, W. Y., Wu, C. L., Pyzocha, L., et al. (2005). NMDA receptors mediate olfactory learning and memory in Drosophila. Curr. Biol. 15, 603-615. doi: 10.1016/j.cub.2005.02.059
61. Xie, Z., Huang, C., Ci, B., Wang, L., and Zhong, Y. (2013). Requirement of the combination of mushroom body y lobe and a/p lobes for the retrieval of both aversive and appetitive early memories in Drosophila. Learn. Mem. 20,474-481. doi: 10.1101/lm.031823.113
62. Zhang, K., Guo, J. Z., Peng, Y., Wang, X., and Gui, A. (2007). Dopamine-mushroom body circuit regulates saliency-based decision making in Drosophila. Science 316, 1901-1904. doi: 10.1126/science.1137357
63. Zhang, X., Qingzhong, R., and Guo, A. (2013). Parallel pathways for cross- modal memory retrieval in Drosophila. J. Neurosci. 33, 8784-8793. doi: 10.1523/JNEUROSCI.4631-12.2013