Local remapping of place cell firing in the Tolman detour task

European Journal of Neuroscience

Volumn 33, Issue 9, 2011, Pages 1696-1705

  Alvernhe, Alice ^a,b   Save, Etienne ^a,b   Poucet, Bruno ^a,b  

^a CNRS   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Hippocampus; Network; Rat; Spatial processing; Unit recordings

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; BRAIN MAPPING; CELL POPULATION; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; MALE; MAZE TEST; MENTAL TASK; NERVE CELL; NONHUMAN; PLACE CELL FIRING; PRIORITY JOURNAL; RAT; REWARD; TASK PERFORMANCE;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; BRAIN MAPPING; HIPPOCAMPUS; MALE; NEURONS; NEUROPSYCHOLOGICAL TESTS; RATS; RATS, LONG-EVANS;

EID: 79955533788     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07653.x     Document Type: Article

References (56)

1. Alvernhe, A., Van Cauter, T., Save, E. & Poucet, B. (2008) Different CA1 and CA3 representations of novel routes in a shortcut situation. J. Neurosci., 28, 7324-7333.
2. Barry, C. & Burgess, N. (2007) Learning in a geometric model of place cell firing. Hippocampus, 17, 786-800.
3. Blum, K.I. & Abbott, L.F. (1996) A model of spatial map formation in the hippocampus of the rat. Neural Comput., 8, 85-93.
4. Cressant, A., Muller, R.U. & Poucet, B. (1997) Failure of centrally placed objects to control the firing field of hippocampal place cells. J. Neurosci., 17, 2531-2542.
5. Cressant, A., Muller, R.U. & Poucet, B. (1999) Further study of the control of place cells firing by intra-apparatus objects. Hippocampus, 9, 423-431.
6. Daumas, S., Halley, H., Francés, B. & Lassalle, J.M. (2005) Encoding, consolidation, and retrieval of contextual memory: differential involvement of dorsal CA1 and CA3 hippocampal subregions. Learn. Mem., 12, 375-382.
7. Eichenbaum, H. & Fortin, N.J. (2005) Bridging the gap between brain and behavior: cognitive and neural mechanisms of episodic memory. J. Exp. Anal. Behav., 84, 619-629.
8. Farovik, A., Dupont, L. & Eichenbaum, H. (2010) Distinct roles for dorsal CA1 and CA3 in memory for sequential nonspatial events. Learn. Mem., 17, 12-17.
9. Gaussier, P., Revel, A., Banquet, J.P. & Babeau, V. (2002) From view cells and place cells to cognitive map learning: processing stages of the hippocampal system. Biol. Cybern., 86, 15-28.
10. Gerstner, W. & Abbott, L.F. (1997) Learning navigational maps through potentiation and modulation of hippocampal place cells. J. Comput. Neurosci., 4, 79-94.
11. Gothard, K.M., Skaggs, W.E., Moore, K.M. & McNaughton, B.L. (1996a) Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J. Neurosci., 16, 823-835.
12. Gothard, K.M., Skaggs, W.E. & McNaughton, B.L. (1996b) Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J. Neurosci., 16, 8027-8040.
13. Gupta, A.S., Van der Meer, M.A.A., Touretzky, D.S. & Redish, A.D. (2010) Hippocampal replay is not a simple function of experience. Neuron, 65, 695-705.
14. Hartley, T., Burgess, N., Lever, C., Cacucci, F. & O'Keefe, J. (2000) Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus, 10, 369-379.
15. Hetherington, P.A. & Shapiro, M.L. (1997) Hippocampal place fields are altered by the removal of single visual cues in a distance-dependent manner. Behav. Neurosci., 111, 20-34.
16. Isaac, J.T.R., Buchanan, K.A., Muller, R.U. & Mellor, J.R. (2009) Hippocampal place cells firing patterns can induce long-term synaptic plasticity in vivo. J. Neurosci., 29, 6840-6850.
17. Jensen, O. & Lisman, J.E. (1996) Hippocampal CA3 region predicts memory sequences: accounting for phase precession of place cells. Learn. Mem., 3, 279-287.
18. Kesner, R.P., Hunsaker, M.R. & Gilbert, P.E. (2005) The role of CA1 in the acquisition of an object-trace-odor paired associate task. Behav. Neurosci., 119, 781-786.
19. Kubie, J.L. (1984) A driveable bundle of microwires for collecting single-unit data from freely moving rats. Physiol. Behav., 32, 115-118.
20. Lee, I. & Kesner, R.P. (2002) Differential contribution of: NMDA receptors in hippocampal subregions to spatial working memory. Nat. Neurosci., 5, 162-168.
21. Lee, I. & Kesner, R.P. (2003) Differential roles of dorsal hippocampal subregions in spatial working memory with short versus intermediate delay. Behav. Neurosci., 117, 1044-1053.
22. Lee, I., Rao, G. & Knierim, J.J. (2004a) A double dissociation between hippocampal subfields: differential time course of CA3 and CA1 place cells for processing changed environments. Neuron, 42, 803-815.
23. Lee, I., Yoganarasimha, D., Rao, G. & Knierim, J.J. (2004b) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature, 430, 456-459.
24. Lenck-Santini, P.P., Save, E. & Poucet, B. (2001) Evidence for a relationship between the firing patterns of hippocampal place cells and rat's performance in a spatial memory task. Hippocampus, 11, 377-390.
25. Lenck-Santini, P.P., Rivard, B., Muller, R.U. & Poucet, B. (2005) Study of CA1 place cell activity and exploratory behavior following spatial and nonspatial changes in the environment. Hippocampus, 15, 356-369.
26. Leutgeb, S., Leutgeb, J.K., Moser, E.I. & Moser, M.B. (2006) Fast rate coding in hippocampal ensembles. Hippocampus, 16, 765-774.
27. Markus, E.J., Qin, Y.L., Leonard, B., Skaggs, W.E., McNaughton, B.L. & Barnes, C.A. (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci., 15, 7079-7094.
28. Meyer, J.A. & Filliat, D. (2003) Map-based navigation in mobile robots - ii. A review of map-learning and path-planning strategies. Cogn. Syst. Res., 4, 283-317.
29. Miyashita, T., Kubik, S., Haghighi, N., Steward, O. & Guzowski, J.F. (2009) Rapid activation of plasticity-associated gene transcription in hippocampal neurons provides a mechanism for encoding one-trial experience. J. Neurosci., 29, 898-906.
30. Muller, R.U. & Kubie, J.L. (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci., 7, 1951-1968.
31. Muller, R.U., Kubie, J.L. & Ranck, J.B. (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci., 7, 1935-1950.
32. Muller, R.U., Kubie, J.L. & Saypoff, R. (1991) The hippocampus as a cognitive graph. Abridged version. Hippocampus, 1, 243-246.
33. Muller, R.U., Stead, M. & Pach, J. (1996) The hippocampus as a cognitive graph. J. Gen. Physiol., 107, 663-694.
34. Nakazawa, K., Quirk, M.C., Chitwood, R.A., Watanabe, M., Yeckel, M.F., Sun, L.D., Kato, A., Carr, C.A., Johnston, D., Wilson, M.A. & Tonegawa, S. (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science, 297, 211-218.
35. Nakazawa, K., Sun, L.D., Quirk, M.C., Rondi-Reig, L., Wilson, M.A. & Tonegawa, S. (2003) Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron, 38, 305-315.
36. O'Keefe, J. & Burgess, N. (1996) Geometric determinants of the place fields hippocampal neurons. Nature, 381, 425-428.
37. O'Keefe, J. & Dostrovsky, J. (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely moving rat. Brain Res., 34, 171-175.
38. O'Keefe, J. & Nadel, L. (1978) Hippocampus as a Cognitive Map. Clarendon, Oxford.
39. O'Keefe, J. & Speakman, A. (1987) Single unit activity in the rat hippocampus during a spatial memory task. Exp. Brain Res., 68, 1-27.
40. Paxinos, G. & Watson, C. (2005) The Rat Brain in Stereotaxic Coordinates, 5th edn. Academic Press, Sydney.
41. Poucet, B. (1993) Spatial cognitive maps in animals: new hypotheses on their structure and neural mechanisms. Psychol. Rev., 100, 163-182.
42. Poucet, B. & Benhamou, S. (1997) The neuropsychology of spatial cognition in the rat. Crit. Rev. Neurobiol., 11, 101-120.
43. Poucet, B., Thinus-Blanc, C. & Chapuis, N. (1983) Route-planning in cats, in relation to the visibility of the goal. Anim. Behav., 31, 594-599.
44. Poucet, B., Lenck-Santini, P.P., Hok, V., Save, E., Banquet, J.P., Gaussier, P. & Muller, R.U. (2004) Spatial navigation and hippocampal place cell firing: the problem of goal encoding. Rev. Neurosci., 15, 89-107.
45. Renaudineau, S., Poucet, B. & Save, E. (2007) Flexible use of proximal objects and distal cues by hippocampal place cells. Hippocampus, 17, 381-395.
46. Rivard, B., Li, Y., Lenck-Santini, P.P., Poucet, B. & Muller, R.U. (2004) Representation of objects in space by two classes of hippocampal pyramidal cell. J. Gen. Physiol., 124, 9-25.
47. Rolls, E.T. & Kesner, R.P. (2006) A computational theory of hippocampal function and empirical tests of the theory. Prog. Neurobiol., 79, 1-48.
48. Schmajuk, N.A. & Thieme, A.D. (1992) Purposive behavior and cognitive mapping: a neural network model. Biol. Cybern., 67, 165-174.
49. Shapiro, M.L., Tanila, H. & Eichenbaum, H. (1997) Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus, 7, 624-642.
50. Siegel, J.J., Neunuebel, J.P. & Knierim, J.J. (2008) Dominance of the proximal coordinate frame in determining the locations of hippocampal place cell activity during navigation. J. Neurophysiol., 99, 60-76.
51. Tolman, E.C. (1948) Cognitive maps in rats and men. Psychol. Rev., 55, 189-208.
52. Tolman, E.C. & Honzik, C.H. (1930) 'Insights' in rats. Univ. Calif. Pub. Psychol., 4, 215-232.
53. Touretzky, D.S. & Redish, A.D. (1996) Theory of rodent navigation based on interacting representations of space. Hippocampus, 6, 247-270.
54. Trullier, O. & Meyer, J.A. (2000) Animal navigation using a cognitive graph. Biol. Cybern., 83, 271-285.
55. Trullier, O., Wiener, S.I., Berthoz, A. & Meyer, J.A. (1997) Biologically based artificial navigation systems: review and prospects. Prog. Neurobiol., 51, 483-544.
56. Vazdarjanova, A. & Guzowski, J.F. (2004) Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J. Neurosci., 24, 6489-6496.