Competition between cue response and place response: A model of rat navigation behaviour

Connection Science

Volumn 17, Issue 1-2, 2005, Pages 167-183

  Chavarriaga, Ricardo ^a   Strösslin, Thomas ^a   Sheynikhovich, Denis ^a   Gerstner, Wulfram ^a  

^a EPFL   (Switzerland)

Author keywords

Action selection; Biometric agents; Cue response; Hippocampus; Place response; Reinforcement learning; Striatum

Indexed keywords

ACTION SELECTION; CUE RESPONSE; HIPPOCAMPUS; PLACE RESPONSE; STRIATUM;

ANIMALS; BIOMETRICS; NAVIGATION; REINFORCEMENT LEARNING;

COMPUTER SIMULATION;

EID: 24144491024     PISSN: 09540091     EISSN: 13600494     Source Type: Journal    
DOI: 10.1080/09540090500138093     Document Type: Article

References (59)

1. A. Arleo and W. Gerstner, "Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity", Biol. Cybernet., 83, pp. 287-299, 2000.
2. A. Arleo, F. Smeraldi and W. Gerstner, "Cognitive navigation based on nonuniform Gabor space sampling, unsupervised growing networks, and reinforcement learning", IEEE Trans. Neural Net., 15, pp. 639-652, 2004.
3. G. Baldasarre, "A modular neural-network model of the basal ganglia's role in learning and selecting motor behaviours", Cognitive Syst. Res., 3, pp. 5-13, 2002.
4. J.L. Bizon, J.S. Han, C. Hudon and M. Gallagher, "Effects of hippocampal cholinergic deafferentation on learning strategy selection in a visible platform version of the water maze", Hippocampus, 13, pp. 676-684, 2003.
5. M.A. Brown and P.E. Sharp, "Simulation of spatial-learning in the Morris water maze by a neural network model of the hippocampal-formation and nucleus accumbens", Hippocampus, 5, pp. 171-188, 1995.
6. N. Burgess, A. Jackson, T. Hartley and J. O'Keefe, "Predictions derived from modelling the hippocampal role in navigation", Biol. Cybernet., 83, pp. 301-312, 2000.
7. N. Burgess, M. Recce and J. O'Keefe, "A model of hippocampal function", Neural Net., 1, pp. 1065-1081, 1994.
8. J.F. Cahill and M.G. Baxter, "Cholinergic and noncholinergic septal neurons modulate strategy selection in spatial learning", Eur. J. Neurosci., 14, pp. 1856-1864, 2001.
9. Q. Chang and P.E. Gold, "Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats", Behav. Brain Res., 144, pp. 19-24, 2003a.
10. Q. Chang and P.E. Gold, "Switching memory systems during learning: changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats", J. Neurosci., 23, pp. 3001-3005, 2003b.
11. G. Chevalier and J.M. Deniau, "Disinhibition as a basic process in the expression of striatal functions", Trends Neurosci., 13, pp. 277-280, 1990.
12. P.J. Colombo and M. Gallagher, "Individual differences in spatial memory and striatal chat activity among young and aged rats", Neurobiol. Learn. Mem., 70, pp. 314-327, 1998.
13. C. Da Cunha, S. Wietzikoski, E.G. Wietzikoski, E. Miyoshi, M.M. Ferro, J.A. Anselmo-Franci and N.S. Canteras, "Evidence for the substantia nigra pars compacta as an essential component of a memory system independent of the hippocampal memory system", Neurobiol. Learn. Mem., 79, pp. 236-242, 2003.
14. J.M. Daniel and C.D. Lee, "Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze", Neurobiol. Learn. Mem., 82, pp. 142-149, 2004.
15. B.D. Devan and N.M. White, "Parallel information processing in the dorsal striatum: relation to hippocampal function", J. Neurosci., 19, pp. 2789-2798, 1999.
16. K. Doya, "Metalearning and neuromodulation", Neural Net., 15, pp. 495-506, 2002.
17. H. Eichenbaum, C. Stewart and R.G. Morris, "Hippocampal representation in place learning", J. Neurosci., 10, pp. 3531-3542, 1990.
18. D.J. Foster, R.G.M. Morris and P. Dayan, "A model of hippocampally dependent navigation, using the temporal difference learning rule", Hippocampus, 10, pp. 1-16, 2000.
19. P. Gaussier, A. Revel, J.P. Banquet and V. Babeau, "From view cells and place cells to cognitive map learning: processing stages of the hippocampal system", Biol. Cybernet., 86, pp. 15-28, 2002.
20. W. Gerstner and L.F. Abbott, "Learning navigational maps through potentiation and modulation of hippocampal place cells", J. Comput. Neurosci., 4, pp. 79-94, 1996.
21. P.E. Gold, "Acetylcholine modulation of neural systems involved in learning and memory", Neurobiol. Learn. Mem., 80, pp. 194-210, 2003.
22. P.E. Gold, "Coordination of multiple memory systems", Neurobiol. Learn. Mem., 82, pp. 230-242, 2004.
23. K. Gurney, T.J. Prescott and P. Redgrave, "A computational model of action selection in the basal ganglia. I. A new functional anatomy", Biol. Cybernet., 84, pp. 401-410, 2001.
24. M.E. Hasselmo, J. Hay, M. Ilyn and A. Gorchetchnikov, "Neuromodulation, theta rhythm and rat spatial navigation", Neural Net., 15, pp. 689-707, 2002.
25. L.S. Janis, M.M. Glasier, Z. Fulop and D.G. Stein, "Intraseptal injections of 192 igg saporin produce deficits for strategy selection in spatial-memory tasks", Behav. Brain Res., 90, pp. 23-34, 1998.
26. M.S. Jog, Y. Kubota, C.I. Connolly, V. Hillegaart and A.M. Graybiel, "Building neural representations of habits", Science, 286, pp. 1745-1749, 1999.
27. J.J. Kim and M.G. Baxter, "Multiple brain-memory systems: the whole does not equal the sum of its parts", Trends Neurosci., 24, pp. 324-330, 2001.
28. D.L. Korol, "Role of estrogen in balancing contributions from multiple memory systems", Neurobiol. Learn. Mem., 82, pp. 309-323, 2004.
29. D.L. Korol, E.L. Malin, K.A. Borden, R.A. Busby and J. Couper-Leo, "Shifts in preferred learning strategy across the estrous cycle in female rats", Horm. Behav., 45, pp. 330-338, 2004.
30. L.K. Marriott and D.L. Korol, "Short-term estrogen treatment in ovariectomized rats augments hippocampal acetylcholine release during place learning", Neurobiol. Learn. Mem., 80, pp. 315-322, 2003.
31. D.B. Matthews, M. Ilgen, A.M. White and P.J. Best, "Acute ethanol administration impairs spatial performance while facilitating nonspatial performance in rats", Neurobiol. Learn. Mem., 72, pp. 169-179, 1999.
32. C.K. McIntyre, L.K. Marriott and P.E. Gold, "Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats", Neurobiol. Learn. Mem., 79, pp. 177-183, 2003.
33. J.W. Mink, "The basal ganglia: focused selection and inhibition of competing motor programs", Prog. Neurobiol., 50, pp. 381-425, 1996.
34. S.J. Mizumori, O. Yeshenko, K.M. Gill and D.M. Davis, "Parallel processing across neural systems: implications for a multiple memory system hypothesis", Neurobiol. Learn. Mem., 82, pp. 278-298, 2004.
35. R.G.M. Morris, "Spatial localization does not require the presence of local cues", Learn. Motiv., 12, pp. 239-260, 1981.
36. J. O'Keefe and L. Nadel, The Hippocampus as a Cognitive Map, Oxford: Clarendon Press, 1978.
37. M.G. Oliveira, O.F. Bueno, A.C. Pomarico and E.B. Gugliano, "Strategies used by hippocampal- and caudate-putamen-lesioned rats in a learning task", Neurobiol. Learn. Mem., 68, pp. 32-41, 1997.
38. M.G. Packard, "Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning", Proc. Natl. Acad. Sci. USA, 96, pp. 12881-12886, 1999.
39. M.G. Packard, R. Hirsh and N.M. White, "Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems", J. Neurosci., 9, pp. 1465-1472, 1989.
40. M.G. Packard and B.J. Knowlton, "Learning and memory functions of the basal ganglia", Ann. Rev. Neurosci., 25, pp. 563-593, 2002.
41. M.G. Packard and J.L. McGaugh, "Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning", Neurobiol. Learn. Mem., 65, pp. 65-72, 1996.
42. J.M. Pearce, A.D.L. Roberts and M. Good, "Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors", Nature, 396, pp. 75-77, 1998.
43. B. Pouzet, W.N. Zhang, J. Feldon and J.N. Rawlins, "Hippocampal lesioned rats are able to learn a spatial position using non-spatial strategies", Behav. Brain Res., 133, pp. 279-291, 2002.
44. K.E. Ragozzino, S. Leutgeb and S.J. Mizumori, "Dorsal striatal head direction and hippocampal place representations during spatial navigation", Exp. Brain Res., 139, pp. 372-376, 2001.
45. M.E. Ragozzino and P.E. Gold, "Glucose injections into the medial septum reverse the effects of intraseptal morphine infusions on hippocampal acetylcholine output and memory", Neuroscience, 68, pp. 981-988, 1995.
46. M. Recce and K.D. Harris, "Memory for places: a navigational model in support of Marr's theory of hippocampal function", Hippocampus, 6, pp. 735-748, 1996.
47. A. Redish, Beyond the Cognitive Map, From Place Cells to Episodic Memory, London: MIT Press-Bradford Books, 1999.
48. A.D. Redish, "The hippocampal debate: Are we asking the right questions?", Behav. Brain Res., 127, pp. 81-98, 2001.
49. A.D. Redish and D.S. Touretzky, "The role of the hippocampus in solving the Morris water maze", Neural Comput., 10, pp. 73-111, 1998.
50. J.P. Schroeder, J.C. Wingard and M.G. Packard, "Post-training reversible inactivation of hippocampus reveals interference between memory systems", Hippocampus, 12, pp. 280-284, 2002.
51. W. Schultz, "Getting formal with dopamine and reward", Neuron, 36, pp. 241-263, 2002.
52. W. Schultz, P. Dayan and P.R. Montague, "A neural substrate of prediction and reward", Science, 275, pp. 1593-1599, 1997.
53. R. Sutton and A.G. Barto, Reinforcement Learning-An Introduction, Cambridge, MA: MIT Press, 1998.
54. E.G. Tolman, "Cognitive maps in rats and men", Psychol. Rev., 55, pp. 189-208, 1948.
55. P. Voorn, L.J. Vanderschuren, H.J. Groenewegen, T.W. Robbins and C.M. Pennartz, "Putting a spin on the dorsal-ventral divide of the striatum", Trends Neurosci., 27, pp. 468-474, 2004.
56. I.Q. Whishaw, J.C. Cassel and L.E. Jarrad, "Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where", J. Neurosci., 15, pp. 5779-5788, 1995.
57. I.Q. Whishaw, G. Mittleman, S.T. Bunch and S.B. Dunnett, "Impairments in the acquisition, retention and selection of spatial navigation strategies after medial caudate-putamen lesions in rats", Behav. Brain Res., 24, pp. 125-138, 1987.
58. N.M. White, "The role of stimulus ambiguity and movement in spatial navigation: a multiple memory systems analysis of location discrimination", Neurobiol. Learn. Mem., 82, pp. 216-229, 2004.
59. N.M. White and R.J. McDonald, "Multiple parallel memory systems in the brain of the rat", Neurobiol. Learn. Mem., 77, pp. 125-184, 2002.