Relationships between place cell firing fields and navigational decisions by rats

Journal of Neuroscience

Volumn 22, Issue 20, 2002, Pages 9035-9047

  Lenck Santini, Pierre Pascal ^a   Muller, Robert U ^b,c   Save, Etienne ^a   Poucet, Bruno ^a  

^a CNRS   (France)

^b SUNY DOWNSTATE MEDICAL CENTER   (United States)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Hippocampus; Place cells; Rat; Spatial memory; Spatial navigation; Unit recordings

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; CELL ACTIVITY; CONTROLLED STUDY; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; SPATIAL ORIENTATION; STIMULUS; TASK PERFORMANCE;

EID: 0037109772     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-20-09035.2002     Document Type: Article

References (45)

1. Barnes CA, Suster MS, Shen J, McNaughton BL (1997) Multistability of cognitive maps in the hippocampus of old rats. Nature 388:272-275.
2. Bures J, Fenton AA, Kaminsky Y, Zinyuk L (1997) Place cells and place navigation. Proc Natl Acad Sci USA 94:343-350.
3. Cho YH, Giese KP, Tanila HT, Silva AJ, Eichenbaum H (1998) Abnormal hippocampal spatial representations in aCaMKIIT286A and CREBaD-mice. Science 279:867-869.
4. Cressant A, Muller RU, Poucet B (1997) Failure of centrally placed objects to control the firing fields of hippocampal place cells. J Neurosci 17:2531-2542.
5. Dudchenko P, Taube JS (1997) Correlation between head direction cell activity and spatial behavior on a radial maze. Behav Neurosci 111:3-19.
6. Eichenbaum H, Stewart C, Morris RGM (1990) Hippocampal representation in spatial learning. J Neurosci 10:3531-3542.
7. Fenton AA, Wesierska M, Kaminski Y, Bures J (1998) Both here and there: Simultaneous expression of autonomous spatial memories in rats. Proc Natl Acad Sci USA 95:11493-11498.
8. Fox SE, Ranck Jr JB (1981) Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp Brain Res 41:399-410.
9. Golob EJ, Stackman RW, Wong AC, Taube JS (2001) On the behavioral significance of head direction cells: Neural and behavioral dynamics during spatial memory tasks. Behav Neurosci 115:285-304.
10. Jarrard LE, Okaichi H, Steward O, Goldschmidt RB (1984) On the role of hippocampal connections in the performance of place and cue tasks: Comparisons with damage to hippocampus. Behav Neurosci 98:946-954.
11. Kentros C, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, Muller RU (1998) Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280:2121-2126.
12. Kubie JL (1984) A drivable bundle of microwires for collecting singleunit data from freely moving rats. Physiol Behav 32:115-118.
13. Lenck-Santini PP, 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.
14. Liu X, Huang LT, Kubie J, Rotenberg A, Rivard B, Cilio MR, Hu Y, Muller RU, Holmes GL (2001) Seizure-induced changes in place cell physiology: Relationship to navigational learning. Soc Neurosci Abstr 27:744.4.
15. McHugh TJ, Blum KI, Tsien JZ, Tonegawa S, Wilson MA (1996) Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87:1339-1349.
16. McNaughton BL, Barnes CA, Rao G, Baldwin J, Rasmussen M (1986) Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information. J Neurosci 6:563-571.
17. Morris RGM (1981) Spatial localization does not require the presence of local cues. Learn Motiv 12:239-260.
18. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
19. Morris RGM, Anderson E, Lynch GG, Baudry M (1986a) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774-776.
20. Morris RGM, Hagan JJ, Rawlins JNP (1986b) Allocentric spatial learning by hippocampectomised rats: A further test of the "spatial mapping" and "working memory" theories of hippocampal function. Q J Exp Psychol 38B:365-395.
21. Moser E, Moser MB, Andersen P (1993) Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci 13:3916-3925.
22. Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7:1951-1968.
23. Muller RU, Kubie JL, Ranck JB (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7:1935-1950.
24. Muller RU, Kubie JL, Bostock EM, Taube JS, Quirk GJ (1991) Spatial firing correlates of neurons in the hippocampal formation of freely moving rats. In: Brain and Space (Paillard J, ed), pp 296-333. London: Oxford UP.
25. O'Keefe J, Conway DH (1980) On the trail of the hippocampal engram. Physiol Psychol 8:229-238.
26. 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.
27. O'Keefe J, Nadel L (1978) The Hippocampus as a Cognitive Map. Oxford: Clarendon.
28. O'Keefe J, Speakman A (1987) Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 68:1-27.
29. Packard MG, McGaugh JL (1996) Inactivation of hippocampus and caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65:65-72.
30. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. New York: Academic.
31. Pearce JM, Roberts ADL, Good M (1998) Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature 396:75-77.
32. Poucet B (1985) Spatial behaviour of cats in cue-controlled environments. Q J Exp Psychol 37B:155-179.
33. Poucet B, Benhamou S (1997) The neuropsychology of spatial cognition in the rat. Crit Rev Neurobiol 11:101-120.
34. Rasmussen M, Barnes CA, McNaughton BL (1989) A systematic test of cognitive mapping, working memory, and temporal discontiguity theories of hippocampal formation. Psychobiology 17:335-348.
35. Rivard B, Poucet B, Muller RU (2000) The effects of removing a barrier on the firing of hippocampal place cells. Soc Neurosci Abstr 25:715.
36. Rossier J, Schenk F, Kaminsky Y, Bures J (2000) The place preference task: A new tool for studying the relation between behavior and place cell activity in rats. Behav Neurosci 114:273-284.
37. Rotenberg A, Muller RU (1997) Variable place-cell coupling to a continuous viewed stimulus: Evidence that the hippocampus acts as a perceptual system. Philos Trans R Soc Lond B Biol Sci 352:1505-1513.
38. Rotenberg A, Mayford M, Hawkins RD, Kandel ER, Muller RU (1996) Mice expressing activated CaMKII lack low frequency LTP and do not form stable place cells in the CA1 region of the hippocampus. Cell 87:1351-1361.
39. Rotenberg A, Abel T, Hawkins RD, Kandel ER, Muller RU (2000) Parallel instabilities of long-term potentiation, place cells, and learning caused by decreased protein kinase A activity. J Neurosci 20:8096-8102.
40. Steele RJ, Morris RGM (1999) Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus 9:118-136.
41. Tanila H, Shapiro M, Eichenbaum H (1997a) Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus 7:613-623.
42. Tanila H, Shapiro M, Gallagher M, Eichenbaum H (1997b) Brain aging: Changes in the nature of information coding by the hippocampus. J Neurosci 17:5155-5166.
43. Trullier O, Shibata R, Mulder AB, Wiener SI (1999) Hippocampal neuronal position selectively remains fixed to room cues only in rats alternating between place navigation and beacon approach tasks. Eur J Neurosci 11:4381-4388.
44. Whishaw IQ, Cassel JC, Jarrard LE (1995) Rats with fimbria-fornix lesions display a place response in a swimming pool: A dissociation between getting there and knowing where. J Neurosci 15:5779-5788.
45. Zinyuk L, Kubik S, Kaminsky Y, Fenton AA, Bures J (2000) Understanding hippocampal activity by using purposeful behavior: Place navigation induces place cell discharge in both task-relevant and taskirrelevant spatial reference frames. Proc Natl Acad Sci USA 97:3771-3776.