The Role of the Hippocampus in Solving the Morris Water Maze

Neural Computation

Volumn 10, Issue 1, 1998, Pages 73-111

  Redish, A David ^a   Touretzky, David S ^a  

^a Carnegie Mellon University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMNESIA; ANIMAL; BIOLOGICAL MODEL; COMPUTER SIMULATION; HIPPOCAMPUS; HUMAN; MAZE TEST; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SLEEP; SWIMMING;

AMNESIA; ANIMALS; COMPUTER SIMULATION; HIPPOCAMPUS; HUMANS; MAZE LEARNING; MODELS, NEUROLOGICAL; SLEEP; SWIMMING;

EID: 0031601127     PISSN: 08997667     EISSN: None     Source Type: Journal    
DOI: 10.1162/089976698300017908     Document Type: Article

References (101)

1. Alvarez, P., & Squire, L. R. (1994). Memory consolidation and the medial temporal lobe: A simple network model. Proceedings of the National Academy of Sciences, U.S.A., 91, 7041-7045.
2. Amaral, D. G. (1993). Emerging principles of intrinsic hippocampal organization. Current Opinion in Neurobiology, 3, 225-229.
3. Blum, K. I., & Abbott, L. F. (1996). A model of spatial map formation in the hippocampus of the rat. Neural Computation, 8(1), 85-93.
4. Bohbot, V., Liu, Z., Thurm, S. L., Nadel, L., & Bures, J. (1996a). Spatial memory? Never without a hippocampus. Society for Neuroscience Abstracts, 22, 1873.
5. Bohbot, V., Otahal, P., Liu, Z., Nadel, L., & Bures, J. (1996b). Electroconvulsive shock and lidocaine reveal rapid consolidation of spatial working memory in the water maze. Proceedings of the National Academy of Sciences, U.S.A., 93, 4016-4019.
6. Bolhuis, J. J., Stewart, C. A., & Forrest, E. M. (1994). Retrograde amnesia and memory reactivation in rats with ibotenate lesions to the hippocampus or subiculum. Quarterly Journal of Experimental Psychology, 475(2), 129-150.
7. Brown, M. A., & Sharp, P. E. (1995). Simulation of spatial learning in the Morris water maze by a neural network model of the hippocampal formation and nucleus accumbens. Hippocampus, 5(3), 171-188.
8. Burgess, N., Recce, M., & O'Keefe, J. (1994). A model of hippocampal function. Neural Networks, 7(6/7), 1065-1081.
9. Buzsáki, G. (1989). Two-stage model of memory trace formation: A role for "noisy" brain states. Neuroscience, 31(3), 551-570.
10. Chapuis, N., & Scardigli, P. (1993). Shortcut ability in hamsters (mesocricetus auratus): The role of environmental and kinesthetic information. Animal Learning and Behavior, 21(3), 255-265.
11. Chen, L. L., Lin, L. H., Green, E. J., Barnes, C. A., & McNaughton, B. L. (1994). Head-direction cells in the rat posterior cortex: I. Anatomical distribution and behavioral modulation. Experimental Brain Research, 101, 8-23.
12. Cho, Y. H., Berracochea, D., & Jaffard, R. (1993). Extended temporal gradient for the retrograde and anterograde amnesia produced by ibotenate entorhinal cortex lesions in mice. Journal of Neuroscience, 13(4), 1759-1766.
13. Chrobak, J. J., & Buzsáki, G. (1994). Selective activation of deep layer (V-VI) retrohippocampal neurons during hippocampal sharp waves in the behaving rat. Journal of Neuroscience, 14(10), 6160-6170.
14. Cohen, N. J., & Eichenbaum, H. (1993). Memory, amnesia, and the hippocampal system. Cambridge, MA: MIT Press.
15. Davis, M., Rainnie, D., & Cassell, M. (1994). Neurotransmission in the rat amygdala related to fear and anxiety. Trends in Neurosciences, 17(5), 208-214.
16. DiMattia, B. V. D., & Kesner, R. P. (1988). Spatial cognitive maps: Differential role of parietal cortex and hippocampal formation. Behavioral Neuroscience, 102(4), 471-480.
17. Eichenbaum, H., Stewart, C., and Morris, R. G. M. (1990). Hippocampal representation in place learning. Journal of Neuroscience, 10(11), 3531-3542.
18. Etienne, A. S. (1992). Navigation of a small mammal by dead reckoning and local cues. Current Directions in Psychological Science, 1(2), 48-52.
19. Finch, D. M. (1993). Hippocampal, subicular, and entorhinal afferents and synaptic integration in rodent cingulate cortex. In B. A. Vogt & M. Gabriel (Eds.), Neurobiology of cingulate cortex and limbic thalamus: A comprehensive handbook (pp. 224-248). Boston: Birkhauser.
20. Gallistel, C. R. (1990). The organization of learning. Cambridge, MA: MIT Press.
21. Gluck, M. A., & Myers, C. E. (1993). Hippocampal mediation of stimulus representation: A computational theory. Hippocampus, 3(4), 491-516.
22. Greenstein, Y. J., Pavlides, C., & Winson, J. 1988. Long-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity. Brain Research, 438, 331-334.
23. Hasselmo, M. E. (1995). Neuromodulation and cortical function: Modeling the physiological basis of behavior. Behavioral and Brain Research, 67(1), 1-27.
24. Hasselmo, M. E., & Schnell, E. (1994). Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: Computational modeling and brain slice physiology. Journal of Neuroscience, 14(6), 3898-3914.
25. Hennevin, E., Hars, B., Maho, C., & Bloch, V. (1995). Processing of learned information in paradoxical sleep: Relevance for memory. Behavioural and Brain Research, 69, 125-135.
26. Hertz, J., Krogh, A., & Palmer, R. G. (1991). Introduction to the theory of neural computation. Reading, MA: Addison-Wesley.
27. Huerta, P. T., & Lisman, J. E. (1993). Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature, 364, 723-725.
28. Koerner, A., Thomas, M. J., Weisend, M. P., & Sutherland, R. J. (1996). Hippocampal-dependent memory consolidation: An evaluation of three hypotheses. Society for Neuroscience Abstracts, 22, 1118.
29. Kolb, B. (1990). Posterior parietal and temporal association cortex. In B. Kolb and R. C. Tees (Eds.), The cerebral cortex of the rat (pp. 459-471). Cambridge, MA: MIT Press.
30. Kolb, B., & Walkey, J. (1987). Behavioural and anatomical studies of the posterior parietal cortex in the rat. Behavioral and Brain Research, 23, 127-145.
31. Kudrimoti, H. S., Skaggs, W. E., Barnes, C. A., McNaughton, B. L., Gerrard, J. L., Suster, M. S., & Weaver, K. L. (1996). REM sleep and the reactivation of recent correlation patterns in hippocampal neuronal ensembles. Society for Neuroscience Abstracts, 22, 1871.
32. Landfield, P. W., & Deadwyler, S. A. (Eds.) (1988). Long-term potentiation: From biophysics to behavior. New York: Alan R. Liss.
33. Larson, J., & Lynch, G. (1989). Theta pattern stimulation and the induction of LTP: The sequence in which synapses are stimulated determines the degree to which they potentiate. Brain Research, 489, 49-58.
34. Larson, J., Wong, D., & Lynch, G. (1986). Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Research, 368, 347-350.
35. Leonard, B., & McNaughton, B. L. (1990). Spatial representation in the rat: Conceptual, behavioral, and neurophysiological perspectives. In R. P. Kesner & D. S. Olton (Eds.), Neurobiology of comparative cognition (pp. 363-422). Hillsdale, NJ: Lawrence Erlbaum Associates.
36. Levy, W. B. (1996). A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus, 6(6), 579-591.
37. Levy, W. B., & Wu, X. (1996). The relationship of local context cues to sequence length memory capacity. Network: Computation in Neural Systems, 7, 371-384.
38. Marr, D. (1971). Simple memory: A theory for archicortex. Philosophical Transactions of the Royal Society of London, Series B, 262, 23-81.
39. McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995). Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychological Review, 102(3), 419-457.
40. McDonald, R. J., & White, N. M. (1994). Parallel information processing in the water maze: Evidence for independent memory systems involving dorsal striatum and hippocampus. Behavioral and Neural Biology, 61, 260-270.
41. McGaugh, J. M. (1966). Time-dependent processes in memory storage. Science, 153, 1351-1358.
42. McNaughton, B. L., Mizumori, S. J. Y., Barnes, C. A., Leonard, B. J., Marquis, M., & Green, E. J. (1994). Cortical representation of motion during unrestrained spatial navigation in the rat. Cerebral Cortex, 4(1), 27-39.
43. Mehta, M. R., Barnes, C. A., & McNaughton, B. L. (in press). An evidence for Hebbian synaptic potentiation in hippocampus during behavior. In M. Mozer, M. Jordan, and T. Petsche (Eds.), Advances in Neural Information Processing, 9. Cambridge, MA: MIT Press.
44. Mittelstaedt, M. L., & Mittelstaedt, H. (1980). Homing by path integration in a mammal. Naturwissenschaften, 67, 566-567.
45. Mogenson, G. J. (1984). Limbic-motor integration - with emphasis on initiation of exploratory and goal-directed locamotion. In R. Bandler (Ed.), Modulation of sensorimotor activity during alterations in behavioral states (pp. 121-138). New York: Alan R. Liss.
46. Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681-683.
47. Morris, R. G. M., Schenk, F., Tweedie, F., and Jarrard, L. E. (1990). Ibotenate lesions of hippocampus and/or subiculum: Dissociating components of allocentric spatial learning. European Journal of Neuroscience, 2, 1016-1028.
48. Muller, R. U., Kubie, J. L., and Saypoff, R. (1991). The hippocampus as a cognitive graph. Hippocampus, 1(3), 243-246.
49. Nadel, L. (Ed.) (1991). The hippocampus and space revisited [Special issue]. Hippocampus, 1(3).
50. O'Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Clarendon Press.
51. O'Keefe, J., & Recce, M. (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus, 3, 317-330.
52. O'Reilly, R. C., & McClelland, J. L. (1994). Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade-off. Hippocampus, 4(6), 661-682.
53. Packard, M. G. (1994). "Place" versus "response" learning debate revisited in the brain. Society for Neuroscience Abstracts, 20, 1016.
54. Packard, M. G., & McGaugh, J. L. (1992). Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: Further evidence for multiple memory systems. Behavioral Neuroscience, 106(3), 439-446.
55. Pavlides, C., Greenstein, J., Grudman, M., & Winson, J. (1988). Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm. Brain Research, 439, 383-387.
56. Pavlides, C., & Winson, J. (1989). Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. Journal of Neuroscience, 9(8), 2907-2918.
57. Pinto, D. J., Brumberg, J. C., Simons, D. J., & Ermentrout, G. B. (1996). A quantitative population model of whisker barrels: Re-examining the Wilson-Cowan equations. Journal of Computational Neuroscience, 3(3), 247-264.
58. Poucet, B., Thinus-blanc, C., & Chapuis, N. (1983). Route planning in cats, in relation to the visibility of the goal. Animal Behavior, 31, 594-599.
59. Redish, A. D., Elga, A. N. & Touretzky, D. S. (1996). A coupled attractor model of the rodent head direction system. Network, 7(4), 671-685.
60. Redish, A. D., & Touretzky, D. S. (1996). Details of a comprehensive theory of rodent navigation. Society for Neuroscience Abstracts, 22, 678.
61. Redish, A. D., & Touretzky, D. S. (1997). Cognitive maps beyond the hippocampus. Hippocampus, 7(1), 15-35.
62. Rempel-Clower, N. L., Zola, S. M., Squire, L. R., & Amaral, D. G. (1996). Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. Journal of Neuroscience, 16, 5233-5255.
63. Rolls, E. T. (1989). The representation and storage of information in neuronal networks in the primate cerebral cortex and hippocampus. In R. Durbin, C. Miall, & G. Mitchison (Eds.), The computing neuron (pp. 125-159). Reading, MA: Addison-Wesley.
64. Rolls, E. T. (1996). A theory of hippocampal function in memory. Hippocampus, 6, 601-620.
65. Rumelhart, D. E., Hinton, G. E., & Williams, R. J. (1986). Learning internal representations by error propogation. In D. E. Rumelhart & J. L. McClelland (Eds.), Parallel distributed processing: Explorations in the microstructure of cognition (volume 1, pp. 318-362). Cambridge, MA: MIT Press.
66. Samsonovich, A., & McNaughton, B. L. (in press). Path integration and cognitive mapping in a continuous attractor model of the hippocampus. Journal of Neuroscience.
67. Schauert, T., Day, L. B., Weisend, M., & Sutherland, R. J. (1996). Spatial learning by hippocampal rats in the Morris water task. Society for Neuroscience Abstracts, 22, 678.
68. Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry, 20, 11-21.
69. Shen, B., & McNaughton, B. L. (1997). Modeling the spontaneous reactivation of experience-specific hippocampal cell assembles during sleep. Hippocampus, 6(6), 685-693.
70. Skaggs, W. E. (1995). Relations between the theta rhythm and activity patterns of hippocampal neurons. Unpublished doctoral dissertation, University of Arizona.
71. Skaggs, W. E., & McNaughton, B. L. (1996). Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science, 271, 1870-1873.
72. Skaggs, W. E., McNaughton, B. L., Wilson, M. A., & Barnes, C. A. (1996). Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus, 6(2), 149-173.
73. Smith, C. (1995). Sleep states and memory processes. Behavioural and Brain Research, 69, 137-145.
74. Squire, L. R. (1992). Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychology Review, 99(2), 195-231.
75. Squire, L. R., & Alvarez, P. (1995). Retrograde amnesia and memory consolidation: A neurobiological perspective. Current Opinion in Neurobiology, 5, 169-177.
76. Squire, L. R., & Zola-Morgan, S. (1988). Memory: Brain systems and behavior. Trends in Neurosciences, 11(4), 170-175.
77. Sripanidkulchai, K., & Wyss, J. M. (1986). Thalamic projections to retrosplenial cortex in the rat. Journal of Comparative Neurology, 254, 143-165.
78. Stewart, M., & Fox, S. E. (1990). Do septal neruons pace the hippocampal theta rhythm? Trends in Neurosciences, 13(5), 163-168.
79. Sutherland, R. J., & Hoesing, J. M. (1993). Posterior cingulate cortex and spatial memory: A microlimnology analysis. In B. A. Vogt & M. Gabriel (Eds.), Neurobiology of cingulate cortex and limbic thalamus: A comprehensive handbook (pp. 461-477). Boston: Birkhauser.
80. Sutton, R. S. (Ed.) (1992). Reinforcement learning [Special issue]. Machine Learning, 8(3/4).
81. Tolman, E. C. (1948). Cognitive maps in rats and men. Psychological Review, 55, 189-208.
82. Touretzky, D. S., & Redish, A. D. (1996). A theory of rodent navigation based on interacting representations of space. Hippocampus, 6(3), 247-270.
83. Tsodyks, M., & Sejnowski, T. J. (1995). Associative memory and hippocampal place cells. International Journal of Neural Systems, 6 (Suppl.), 81-86.
84. Tsodyks, M. V., Skaggs, W. E., Sejnowski, T. J., & McNaughton, B. L. (1996). Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model. Hippocampus, 6(3), 271-280.
85. van Groen, T., Vogt, B. A., & Wyss, J. M. (1993). Interconnections between the thalamus and retrosplenial cortex in the rodent brain. In B. A. Vogt & M. Gabriel (Eds.), Neurobiology of cingulate cortex and limbic thalamus: A comprehensive handbook (pp. 123-150). Boston: Birkhauser.
86. Vanderwolf, C. H. (1971). Limbic-diencephalic mechanisms of voluntary movement. Psychological Review, 78(2), 83-113.
87. Vanderwolf, C. H. (1990). An introduction to the electrical activity of the cerebral cortex: Relations to behavior and control by subcortical inputs. In B. Kolb & R. C. Tees (Eds.), The cerebral cortex of the rat (pp. 151-189). Cambridge, MA: MIT Press.
88. Vanderwolf, C. H., & Leung, (1983). Hippocampal rhythmical slow activity: A brief history and the effects of entorhinal lesions and phencyclidine. In W. Seifert (Ed.), Neurobiology of the hippocampus (pp. 275-302). New York: Academic Press.
89. Vogt, B. A. (1985). Cingulate cortex. In A. Peters & E. Jones (Eds.), Association and auditory cortices (pp. 89-150). New York: Plenum Press.
90. Weisend, M. P., Astur, R. S., & Sutherland, R. J. (1996). The specificity and temporal characteristics of retrograde amnesia after hippocampal lesions. Society for Neuroscience Abstracts, 22, 1118.
91. Whishaw, I. Q., Cassel, J-C., & Jarrard, L. E. (1995). Rats with fimbria-fornix lesions display a place response in a swimming pool: A dissociation between getting there and knowing where. Journal of Neuroscience, 15(8), 5779-5788.
92. Wilson, H. R., & Cowan, J. D. (1972). Excitatory and inhibitory interactions in localized populations of model neurons. Biophysical Journal, 22(1), 1-24.
93. Wilson, M. A., & McNaughton, B. L. (1994). Reactivation of hippocampal ensemble memories during sleep. Science, 265, 676-679.
94. Winocur, G. (1990). Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions. Behavioural and Brain Research, 38, 145-154.
95. Witter, M. P. (1993). Organization of the entorhinal-hippocampal system: A review of current anatomical data. Hippocampus, 3, 33-44.
96. Witter, M. P., Ostendorf, R. H., & Groenwegen, H. J. (1990). Heterogeneity in the dorsal subiculum of the rat. Distinct neuronal zones project to different cortical and subcortical targets. European Journal of Neuroscience, 2, 718-725.
97. Wood, E. R., Mumby, D. G., Pinel, J. P. J., & Phillips, A. G. (1996). Impaired object recognition memory in rats following ischemia-induced damage to the hippocampus. Behavioral Neuroscience, 207(1), 51-62.
98. Wu, X., Baxter, R. A., & Levy, W. B. (1996). Context codes and the effect of noisy learning on a simplified hippocampal CA3 model. Biological Cybernetics, 74, 159-165.
99. Wyss, J. M., & van Groen, T. (1992). Connections between the retrosplenial cortex and the hippocampal formation in the rat: A review. Hippocampus, 2(1), 1-12.
100. Zhang, K. (1996). Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: A theory. Journal of Neuroscience, 16(6), 2112-2126.
101. Zola-Morgan, S., & Squire, L. R. (1993). Neuroanatomy of memory. Annual Review of Neuroscience, 16, 547-563.