Neuronal computations underlying the firing of place cells and their role in navigation

Hippocampus

Volumn 6, Issue 6, 1996, Pages 749-762

  Burgess, Neil ^a   O'Keefe, John ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Hippocampus; Model; Network; Rat; Spatial

Indexed keywords

ARTICLE; CELL ACTIVITY; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; NERVE CELL; NONHUMAN; PREDICTION; PRIORITY JOURNAL; RAT; SPATIAL MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; EVALUATION STUDIES; HIPPOCAMPUS; LEARNING; MODELS, NEUROLOGICAL; NEURONS; RATS; SPATIAL BEHAVIOR;

EID: 0030499770     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1063(1996)6:6<749::AID-HIPO16>3.0.CO;2-0     Document Type: Article

References (72)

1. Aguirre GK, Detre JA, D'Esposito M, Alsop D, Rosenquist AC (1995) Maze navigation activates the hippocampal formation during learning and recall: a fMRI study. Soc Neurosci Abstr 21(116.2):272.
2. Arolfo MP, Nerad L, Schenk F, Bures J (1994) Absence of snapshot memory of the target view interferes with place learning by rats in the water maze. Behav Neurosci 108:308-316.
3. Barnes CA, McNaughton BL, Mizumori SJY, Leonard BW, Lin L-H (1990) Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog Brain Res 83:287-300.
4. Benhamou S, Seguinot V (1995) How to find ones way in the labyrinth of path integration models. J Theor Biol 174:463-466.
5. Blum KI, Abbott LF (1995) Functional significance of long term potentiation in recurrent netwarks. Int J Neural Syst [Suppl] 6:25-31.
6. Brown MF (1992) Does a cognitive map guide choice in the radial-arm maze? J Exp Psychol 18:56-66.
7. Brown MA, Sharp PE (1995) Simulation of spatial learning in the Morris water maze by a neural netwark model of the hippocampal formation and nucleus accumbens. Hippocampus 5:171-188.
8. Burgess N, O'Keefe J (1995) Modelling spatial navigation by the rat hippocampus. Int J Neural Syst [Suppl] 6:87-94.
9. Burgess N, O'Keefe J, Recce M (1993) Using hippocampal 'place cells' for navigation, exploiting phase coding. In: Advances in neural information processing systems 5 (Hanson SJ, Giles CL, Cowan JD, eds), pp 929-936. San Mateo, CA: Morgan Kaufmann.
10. Burgess N, Recce M, O'Keefe J (1994) A model of hippocampal function. Neural Networks 7:1065-1081.
11. Burgess N, Recce M, O'Keefe J (1995) Hippocampus - spatial models. In: The handbook of brain theory and neural networks (Arbib MA, ed), pp 468-472. Cambridge, MA: MIT Press.
12. Burgess N, Donnett JG, O'Keefe J (1996) Modelling navigation by the rat hippocampus. Forma 11:83-101.
13. Chen LL, Lin LH, Green EJ, Barnes CA, McNaughton BL (1994) Head-direction cells in the rat posterior cortex. 1. Anatomical distribution and behavioral modulation. Exp Brain Res 101:8-23.
14. Eichenbaum H, Otto T, Cohen NJ (1994) 2 functional components of the hippocampal memory system. Behav Brain Sci 17:449-472.
15. Feigenbaum JD, Polkey CE, Morris RG (1996) Deficits in spatial working-memory after unilateral temporal lobectomy in man. Neuropsychologia 34:163-176.
16. Fox SE, Wolfson S, Ranck JB (1986) Hippocampal theta-rhythm and the firing of neurons in walking and urethane anesthetized rats. Exp Brain Res 62:495-508.
17. Georgopoulos AP, Kettner RE, Schwartz AB (1988) Primate motor cortex and free arm movements to visual targets in three-dimensional space. II. Coding of the direction of movement by a neuronal population. J Neurosci 8:2928-2937.
18. Gothard KM, Skaggs WE, McNaughton BL (1996) Binding of hippocampal CA1 neural activity to multiple reference frame in a landmark-based navigation task. J Neurosci 16:823-835.
19. Harley CW (1979) Arm choices in a sunburst maze: effects of hippocampectomy in the rat. Physiol Behav 23:283-290.
20. Hetherington PA, Shapiro ML (1993) A simple netwark model simulates hippocampal place fields: II. Computing goal-directed trajectories and memory fields. Behav Neurosci 107:434-443.
21. Hill AJ (1978) First occurrence of hippocampal spatial firing in a new environment. Expl Neurol 62:282-297.
22. Jarrard LE (1993) On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 60:9-26.
23. Jung MW, Wiener SI, McNaughton BL (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14:7347-7356.
24. Levy WB (1996) A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal problems. Hippocampus 6:579-590.
25. Macrides F (1975) Temporal relationship betwaen hippocampal slow waves and exploratory sniffing in hamsters. Behav Biol 14:295-308.
26. Maguire EA, Burke T, Phillips J, Staunton H (1996) Topographical disorientation following unilateral temporal lobe lesions in humans. Neuropsychologia 34:993-1001.
27. McNaughton BL, Barnes CA, O'Keefe J (1983) The contribution of position, direction and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52:41-49.
28. McNaughton BL, Knierim JJ, Wilson MA (1995) Vector encoding and the vestibular foundations of spatial cognition: a neurophysiological and computational hypothesis. In: The cognitive neurosciences (Gazzaniga M, ed), pp 585-595. Boston: MIT Press.
29. McNaughton BL, Barnes CA, Gerrard JL, Gothard KM, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL (1996) Deciphering the hippocampal polyglot - the hippocampus as a path integration system. J Exp Biol 199:173-185.
30. Mizumori SJY, Williams JD (1993) Directionally sensitive mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13:4015-4028.
31. Morris RGM (1981) Spatial localisation does not depend on the presence of local cues. Learning Motivation 12:239-260.
32. Morris RGM, Garrard P, Rawlins JNP, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
33. 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.
34. Muller RU, Kubie JL, Ranck JB (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7:1935-1950.
35. Muller RU, Kubie JL, Bostock EM, Taube JS, Quirk GJ (1991a) Spatial firing correlates of neurons in the hippocampal formation of freely moving rats. In: Brain and space (Paillard J, ed), pp 296-333. UK: Oxford University Press.
36. Muller RU, Kubie JL, Saypoff R (1991b) The hippocampus as a cognitive graph. Hippocampus 1:243-246.
37. Muller RU, Bostock E, Taube JS, Kubie JL (1994) On the directional firing properties of hippocampal place cells. J Neurosci 14:7235-7251.
38. Murray EA, Davidson M, Gaffan D, Olton DS, Suomi S (1989) Effects of fornix transection and cingulate cortical ablation on spatial memory in rhesus monkeys. Exp Brain Res 74:173-186.
39. Nicolelis MA, Chapin JK (1994) Spatiotemporal structure of somatosensory responses of many-neuron ensembles in the rat ventral posterior medial nucleus of the thalamus. J Neurosci 14:3511-3532.
40. O'Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78-109.
41. O'Keefe J (1991) The hippocampal cognitive map and navigational strategies. In: Brain and space (Paillard J, ed), pp 273-295. Oxford: Oxford University Press.
42. O'Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425-428.
43. O'Keefe J, Conway DH (1978) Hippocampal place units in the freely moving rat: why they fire where they fire. Exp Brain Res 31:573-590.
44. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford: Oxford University Press.
45. O'Keefe J, Recce M (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
46. O'Keefe J, Speakman A (1987) Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 68:1-27.
47. O'Keefe J, Nadel L, Keightley S, Kill D (1975) Fornix lesions selectively abolish place learning in the rat. Exp Neurol 48:152-166.
48. Olton DS, Walker JA Gage H (1978) Hippocampal connections and spatial discrimination. Brain Res 139:295-308.
49. Parkinson JK, Murray EA, Mishkin M (1988) A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects. J Neurosci 8:4159-4167.
50. Pavlides C, Greenstein YJ, Grudman M, Winson J (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm. Brain Res 439:383-387.
51. Poucet B, Thinus-Blanc C, Muller RU (1994) Place cells in the ventral hippocampus of rats. Neuroreport 5:2045-2048.
52. Quirk GJ, Muller RU, Kubie JL, Ranck JB (1992) The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12:1945-1963.
53. Recce M, Harris KD (1996) Memory for places: a navigational model in support of Marr's theory of hippocampal function. Hippocampus 6:735-748.
54. Redish AD, Touretzky DS (1996) Navigating with landmarks: computing goal locations from place codes. In: Symbolic visual learning (Ikeuchi K, Veloso M, eds), Oxford: Oxford University Press, in press.
55. Rumelhart DE, Zipser D (1986) Feature discovery by competitive learning. In: Parallel distributed processing 1 (Rumelhart DE, McClelland JL, eds), pp 151-193. Cambridge, MA: MIT Press.
56. Rumelhart DE, Hinton GE, Williams RJ (1986) Learning internal representations by error propagation. In: Parallel distributed processing 1 (Rumelhart DE, McClelland JL, eds), pp 318-362. Cambridge, MA: MIT Press.
57. Shapiro ML, Hetherington PA(1993) A simple network model simulates hippocampal place fields: I. parametric analyses and physiological predictions. Behav Neurosci 107:34-50.
58. Sharp PE (1991) Computer simulation of hippocampal place cells. Psychobiology 19:103-115.
59. Sharp PE, Green C (1994) Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J Neurosci 14:2339-2356.
60. Sharp PE, Blair HT, Brown MA (1996) Neural network modeling of the hippocampal formation spatial signals, and their possible role in navigation: a modular approach. Hippocampus 6:720-734.
61. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.
62. Smith ML, Leonard G, Crane J, Milner B (1995) The effects of frontal-lobe or temporal-lobe lesions - on susceptibility to interference in spatial memory Neuropsychologia 33:275-285.
63. Squire LR (1992) Declarative and nondeclarative memory multiple brain systems supporting learning and memory. J Cog Neurosci 4:232-243.
64. Sutherland RJ, Chew GL, Baker JC, Linggard RC (1987) Some limitations on the use of distal cues in place navigation by rats. Psychobiology 15:48-57.
65. Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70-86.
66. Taube JS, Muller RU, Ranck JB (1990) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10:420-435.
67. Tesche CD (1995) Noninvasive detection of theta activity in human hippocampal formation with a whole-head magnetoencephalographic array Soc Neurosci Abstr 21(117.11):276.
68. Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189-208.
69. Treves A, Miglino O, Parisi D (1992) Rats, nets, maps, and the emergence of place cells. Psychobiology 20:1-8.
70. Whishaw IQ (1991) Latent learning in a swimming pool place task by rats - evidence for the use of associative and not cognitive mapping processes. Q J Exp Psychol B 43:83-103.
71. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261:1055-1058.
72. Zipser D (1985) A computational model of hippocampal place fields. Behav Neurosci 99:1006-1018.