An attractor network in the hippocampus: Theory and neurophysiology

Learning and Memory

Volumn 14, Issue 11, 2007, Pages 714-731

  Rolls, Edmund T ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIOR; CA3 SYSTEM; DENTATE GYRUS; ENTORHINAL CORTEX; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; MOSSY FIBER; NEOCORTEX; NERVE CELL NETWORK; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RECALL; REVIEW; REWARD;

ANIMALS; HIPPOCAMPUS; HUMANS; MEMORY; MODELS, NEUROLOGICAL; NONLINEAR DYNAMICS;

EID: 36448971226     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.631207     Document Type: Review

References (159)

1. Amaral, D.G. 1987. Memory: Anatomical organization of candidate brain regions. In Handbook of physiology, Section 1: The nervous system (ed. V.B. Moutcastle), pp. 211-294. American Physiological Society, Washington, DC.
2. Amaral, D.G. 1993. Emerging principles of intrinsic hippocampal organisation. Curr. Opin. Neurobiol. 3: 225-229.
3. Amaral, D.G. and Witter, M.P. 1989. The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience 31: 571-591.
4. Amaral, D.G. and Witter, M.P. 1995. The hippocampal formation. In The Rat nervous system (ed. G. Paxinos), pp. 443-493. Academic Press, San Diego.
5. Amaral, D.G., Ishizuka, N., and Claiborne, B. 1990. Neurons, numbers and the hippocampal network. Prog. Brain Res. 83: 1-11.
6. Amaral, D.G., Price, J.L., Pitkanen, A., and Carmichael, S.T. 1992. Anatomical organization of the primate amygdaloid complex. In The amygdala (ed. J.P. Aggleton), pp. 1-66. Wiley-Liss, New York.
7. Amari, S. 1977. Dynamics of pattern formation in lateral-inhibition type neural fields. Biol. Cybern. 27: 77-87.
8. Amit, D.J. 1989. Modeling brain function. Cambridge University Press, Cambridge.
9. Battaglia, F.P. and Treves, A. 1998a. Attractor neural networks storing multiple space representations: A model for hippocampal place fields. Phys. Rev. E 58: 7738-7753.
10. Battaglia, F.P. and Treves, A. 1998b. Stable and rapid recurrent processing in realistic auto-associative memories. Neural Comput. 10: 431-450.
11. Brown, T.H., Ganong, A.H., Kairiss, E.W., Keenan, C.L., and Kelso, S.R., eds. 1989. Long-term potentiation in two synaptic systems of the hippocampal brain slice. Academic Press, San Diego.
12. Brown, T.H., Kairiss, E.W., and Keenan, C.L. 1990. Hebbian synapses: Biophysical mechanisms and algorithms. Annu. Rev. Neurosci. 13: 475-511.
13. Brun, V.H., Otnass, M.K., Molden, S., Steffenach, H.A., Witter, M.P., Moser, M.B., and Moser, E.I. 2002. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296: 2243-2246.
14. Buckley, M.J. and Gaffan, D. 2000. The hippocampus, perirhinal cortex, and memory in the monkey. In Brain, perception, and memory: Advances in cognitive neuroscience (ed. J.J. Bolhuis), pp. 279-298. Oxford University Press, Oxford.
15. Burgess, N., Maguire, E.A., and O'Keefe, J. 2002. The human hippocampus and spatial and episodic memory. Neuron 35: 625-641.
16. Carmichael, S.T. and Price, J.L. 1995. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J. Comp. Neurol. 346: 403-434.
17. Cassaday, H.J. and Rawlins, J.N. 1997. The hippocampus, objects, and their contexts. Behav. Neurosci. 111: 1228-1244.
18. Chawla, M.K., Guzowski, J.F., Ramirez-Amaya, V., Lipa, P., Hoffman, K.L., Marriott, L.K., Worley, P.F., McNaughton, B.L., and Barnes, C.A. 2005. Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15: 579-586.
19. Crane, J. and Milner, B. 2005. What went where? Impaired object-location learning in patients with right hippocampal lesions. Hippocampus 15: 216-231.
20. Day, M., Langston, R., and Morris, R.G. 2003. Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 424: 205-209.
21. de Araujo, I.E.T., Rolls, E.T., and Stringer, S.M. 2001. A view model which accounts for the spatial fields of hippocampal primate spatial view cells and rat place cells. Hippocampus 11: 699-706.
22. Delatour, B. and Witter, M.P. 2002. Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways. Eur. J. Neurosci. 15: 1400-1407.
23. Fazeli, M.S. and Collingridge, G.L., eds. 1996. Cortical plasticity: LTP and LTD. Bios, Oxford.
24. Feigenbaum, J.D. and Rolls, E.T. 1991. Allocentric and egocentric spatial information processing in the hippocampal formation of the behaving primate. Psychobiology 19: 21-40.
25. Florian, C. and Roullet, P. 2004. Hippocampal CA3-region is crucial for acquisition and memory consolidation in Morris water maze task in mice. Behav. Brain Res. 154: 365-374.
26. Franco, L., Rolls, E.T., Aggelopoulos, N.C., and Jerez, J.M. 2007. Neuronal selectivity, population sparseness, and ergodicity in the inferior temporal visual cortex. Biol. Cybern. 96: 547-560. doi: 10.1007/s00422-007-0149-1.
27. Fyhn, M., Molden, S., Witter, M.P., Moser, E.I., and Moser, M.B. 2004. Spatial representation in the entorhinal cortex. Science 305: 1258-1264.
28. Gaffan, D. 1994. Scene-specific memory for objects: A model of episodic memory impairment in monkeys with fornix transection. J. Cogn. Neurosci. 6: 305-320.
29. Gaffan, D. and Harrison, S. 1989a. A comparison of the effects of fornix section and sulcus principalis ablation upon spatial learning by monkeys. Behav. Brain Res. 31: 207-220.
30. Gaffan, D. and Harrison, S. 1989b. Place memory and scene memory: Effects of fornix transection in the monkey. Exp. Brain Res. 74: 202-212.
31. Gaffan, D. and Saunders, R.C. 1985. Running recognition of configural stimuli by fornix transected monkeys. Q. J. Exp. Psychol. B 37: 61-71.
32. Georges-François, P., Rolls, E.T., and Robertson, R.G. 1999. Spatial view cells in the primate hippocampus: Allocentric view not head direction or eye position or place. Cereb. Cortex 9: 197-212.
33. Gilbert, P.E., Kesner, R.P., and Lee, I. 2001. Dissociating hippocampal subregions: Double dissociation between dentate gyrus and CA1. Hippocampus 11: 626-636.
34. Gold, A.E. and Kesner, R.P. 2005. The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus 15: 808-814.
35. Goodrich-Hunsaker, N.J., Hunsaker, M.R., and Kesner, R.P. 2005. Effects of hippocampus sub-regional lesions for metric and topological spatial information processing. In Abstract viewer/itinerary planner, program no. 647.1. Society for Neuroscience, Washington, DC.
36. Hafting, T., Fyhn, M., Molden, S., Moser, M.B., and Moser, E.I. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436: 801-806.
37. Hargreaves, E.L., Rao, G., Lee, I., and Knierim, J.J. 2005. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308: 1792-1794.
38. Hasselmo, M.E., Schnell, E., and Barkai, E. 1995. Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J. Neurosci. 15: 5249-5262.
39. Hertz, J., Krogh, A., and Palmer, R.G. 1991. An introduction to the theory of neural computation. Addison-Wesley, Wokingham, UK.
40. Hölscher, C., Jacob, W., and Mallot, H.A. 2003. Reward modulates neuronal activity in the hippocampus of the rat. Behav. Brain Res. 142: 181-191.
41. Ishizuka, N., Weber, J., and Amaral, D.G. 1990. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J. Comp. Neurol. 295: 580-623.
42. Jarrard, E.L. 1993. On the role of the hippocampus in learning and memory in the rat. Behav. Neural Biol. 60: 9-26.
43. Jeffery, K.J. and Hayman, R. 2004. Plasticity of the hippocampal place cell representation. Rev. Neurosci. 15: 309-331.
44. Jeffery, K.J., Anderson, M.I., Hayman, R., and Chakraborty, S. 2004. A proposed architecture for the neural representation of spatial context. Neurosci. Biobehav. Rev. 28: 201-218.
45. Jung, M.W. and McNaughton, B.L. 1993. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3: 165-182.
46. Kesner, R.P. 1998. Neural mediation of memory for time: Role of hippocampus and medial prefrontal cortex. Psychol. Bull. Rev. 5: 585-596.
47. Kesner, R.P. 2007. Behavioral functions of the CA3 subregion of the hippocampus. Learn. Mem. (this issue). doi: 10.1101/lm.688207.
48. Kesner, R.P. and Rolls, E.T. 2001. Role of long term synaptic modification in short term memory. Hippocampus 11: 240-250.
49. Kesner, R.P., Lee, I., and Gilbert, P. 2004. A behavioral assessment of hippocampal function based on a subregional analysis. Rev. Neurosci. 15: 333-351.
50. Kesner, R.P., Hunsaker, M.R., and Warthen, M.W. 2007. CA3 mediates arbitrary associations and episodic memory processing based on performance of reciprocal object place recall tasks. Society for Neuroscience Abstracts, Washington, DC.
51. Lassalle, J.M., Bataille, T., and Halley, H. 2000. Reversible inactivation of the hippocampal mossy fiber synapses in mice impairs spatial learning, but neither consolidation nor memory retrieval, in the Morris navigation task. Neurobiol. Learn. Mem. 73: 243-257.
52. Lavenex, P. and Amaral, D.G. 2000. Hippocampal-neocortical interaction: A hierarchy of associativity. Hippocampus 10: 420-430.
53. Lavenex, P., Suzuki, W.A., and Amaral, D.G. 2004. Perirhinal and parahippocampal cortices of the macaque monkey: Intrinsic projections and interconnections. J. Comp. Neurol. 472: 371-394.
54. Levy, W.B. 1989. A computational approach to hippocampal function. In Computational models of learning in simple neural systems (eds. R.D. Hawkins and G.H. Bower), pp. 243-305. Academic Press, San Diego.
55. Levy, W.B. and Desmond, N.L. 1985. The rules of elemental synaptic plasticity. In Synaptic modification, neuron selectivity, and nervous system organization (eds. W.B. Levy et al.), pp. 105-121. Erlbaum, Hillsdale, NJ.
56. Levy, W.B., Colbert, C.M., and Desmond, N.L. 1990. Elemental adaptive processes of neurons and synapses: A statistical/computational perspective. In Neuroscience and connectionist theory (eds. M.A. Gluck and D.E. Rumelhart), pp. 187-235. Erlbaum, Hillsdale, NJ.
57. Lynch, M.A. 2004. Long-term potentiation and memory. Physiol. Rev. 84: 87-136.
58. Maaswinkel, H., Jarrard, L.E., and Whishaw, I.Q. 1999. Hippocampectomized rats are impaired in homing by path integration. Hippocampus 9: 553-561.
59. Malkova, L. and Mishkin, M. 2003. One-trial memory for object-place associations after separate lesions of hippocampus and posterior parahippocampal region in the monkey. J. Neurosci. 23: 1956-1965.
60. Markus, E.J., Qin, Y.L., Leonard, B., Skaggs, W., McNaughton, B.L., and Barnes, C.A. 1995. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci. 15: 7079-7094.
61. Marr, D. 1971. Simple memory: A theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 262: 23-81.
62. Martin, S.J., Grimwood, P.D., and Morris, R.G. 2000. Synaptic plasticity and memory: An evaluation of the hypothesis. Annu. Rev. Neurosci. 23: 649-711.
63. McClelland, J.L., McNaughton, B.L., and 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. Psychol. Rev. 102: 419-457.
64. McNaughton, B.L. 1991. Associative pattern completion in hippocampal circuits: New evidence and new questions. Brain Res. Brain Res. Rev. 16: 193-220.
65. McNaughton, B.L. and Morris, R.G.M. 1987. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 10: 408-415.
66. McNaughton, B.L. and Nadel, L. 1990. Hebb-Marr networks and the neurobiological representation of action in space. In Neuroscience and connectionist theory (eds. M.A. Gluck and D.E. Rumelhart). Erlbaum, Hillsdale, NJ.
67. McNaughton, B.L., Barnes, C.A., and O'Keefe, J. 1983. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp. Brain Res. 52: 41-49.
68. McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I., and Moser, M.-B. 2006. Path integration and the neural basis of the 'cognitive map.' Nat. Rev. Neurosci. 7: 663-678.
69. Morris, R.G.M. 1989. Does synaptic plasticity play a role in information storage in the vertebrate brain? In Parallel distributed processing: Implications for psychology and neurobiology (ed. R.G.M. Morris), pp. 248-285. Oxford University Press, Oxford.
70. Morris, R.G. 2003. Long-term potentiation and memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 643-647.
71. Morris, R.G., Moser, E.I., Riedel, G., Martin, S.J., Sandin, J., Day, M., and O'Carroll, C. 2003. Elements of a neurobiological theory of the hippocampus: The role of activity-dependent synaptic plasticity in memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 773-786.
72. Moscovitch, M., Rosenbaum, R.S., Gilboa, A., Addis, D.R., Westmacott, R., Grady, C., McAndrews, M.P., Levine, B., Black, S., Winocur, G., et al. 2005. Functional neuroanatomy of remote episodic, semantic and spatial memory: A unified account based on multiple trace theory. J. Anat. 207: 35-66.
73. Moser, E.I. 2004. Hippocampal place cells demand attention. Neuron 42: 183-185.
74. Moser, M.B. and Moser, E.I. 1998. Functional differentiation in the hippocampus. Hippocampus 8: 608-619.
75. Muller, R.U., Kubie, J.L., Bostock, E.M., Taube, J.S., and Quirk, G.J. 1991. Spatial firing correlates of neurons in the hippocampal formation of freely moving rats. In Brain and space (ed. J. Paillard), pp. 296-333. Oxford University Press, Oxford.
76. Muller, R.U., Ranck Jr., J.B., and Taube, J.S. 1996. Head direction cells: Properties and functional significance. Curr. Opin. Neurobiol. 6: 196-206.
77. Murray, E.A., Baxter, M.G., and Gaffan, D. 1998. Monkeys with rhinal cortex damage or neurotoxic hippocampal lesions are impaired on spatial scene learning and object reversals. Behav. Neurosci. 112: 1291-1303.
78. Naber, P.A., Lopes da Silva, F.H., and Witter, M.P. 2001. Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum. Hippocampus 11: 99-104.
79. 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., et al. 2002. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297: 211-218.
80. Oja, E. 1982. A simplified neuron model as a principal component analyser. J. Math. Biol. 15: 267-273.
81. O'Keefe, J. 1984. Spatial memory within and without the hippocampal system. In Neurobiology of the hippocampus (ed. W. Seifert), pp. 375-403. Academic Press, London.
82. O'Keefe, J. and Dostrovsky, J. 1971. The hippocampus as a spatial map: Preliminary evidence from unit activity in the freely moving rat. Brain Res. 34: 171-175.
83. O'Keefe, J. and Nadel, L. 1978. The hippocampus as a cognitive map. Clarendon Press, Oxford.
84. O'Reilly, R.C. and Rudy, J.W. 2001. Conjunctive representations in learning and memory: Principles of cortical and hippocampal function. Psychol. Rev. 108: 311-345.
85. Panzeri, S., Rolls, E.T., Battaglia, F., and Lavis, R. 2001. Speed of information retrieval in multilayer networks of integrate-and-fire neurons. Network Comput. Neural Syst. 12: 423-440.
86. Parkinson, J.K., Murray, E.A., and Mishkin, M. 1988. A selective mnemonic role for the hippocampus in monkeys: Memory for the location of objects. J. Neurosci. 8: 4159-4167.
87. Petrides, M. 1985. Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia 23: 601-614.
88. Pitkanen, A., Kelly, J.L., and Amaral, D.G. 2002. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the entorhinal cortex in the macaque monkey. Hippocampus 12: 186-205.
89. Ranck, J.B.J. 1985. Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. In Electrical activity of the archicortex (eds. G. Buzsaki and C.H. Vanderwolf), pp. 217-220. Akademiai Kiado, Budapest.
90. Rawlins, J.N.P. 1985. Associations across time: The hippocampus as a temporary memory store. Behav. Brain Sci. 8: 479-496.
91. Robertson, R.G., Rolls, E.T., and Georges-François, P. 1998. Spatial view cells in the primate hippocampus: Effects of removal of view details. J. Neurophysiol. 79: 1145-1156.
92. Robertson, R.G., Rolls, E.T., Georges-François, P., and Panzeri, S. 1999. Head direction cells in the primate pre-subiculum. Hippocampus 9: 206-219.
93. Rolls, E.T. 1987. Information representation, processing and storage in the brain: Analysis at the single neuron level. In The neural and molecular bases of learning (eds. J.-P. Changeux and M. Konishi), pp. 503-540. Wiley, Chichester.
94. Rolls, E.T. 1989a. Functions of neuronal networks in the hippocampus and cerebral cortex in memory. In Models of brain function (ed. R.M.J. Cotterill), pp. 15-33. Cambridge University Press, Cambridge.
95. Rolls, E.T. 1989b. Functions of neuronal networks in the hippocampus and neocortex in memory. In Neural models of plasticity: Experimental and theoretical approaches (eds. J.H. Byrne and W.O. Berry), pp. 240-265. Academic Press, San Diego.
96. Rolls, E.T. 1989c. The representation and storage of information in neuronal networks in the primate cerebral cortex and hippocampus. In The computing neuron (eds. R. Durbin et al.), pp. 125-159. Addison-Wesley, Wokingham, UK.
97. Rolls, E.T. 1990a. Functions of the primate hippocampus in spatial processing and memory. In Neurobiology of comparative cognition (eds. D.S. Olton and R.P. Kesner), pp. 339-362. Erlbaum, Hillsdale, NJ.
98. Rolls, E.T. 1990b. Theoretical and neurophysiological analysis of the functions of the primate hippocampus in memory. Cold Spring Harb. Symp. Quant. Biol. 55: 995-1006.
99. Rolls, E.T. 1991. Functions of the primate hippocampus in spatial and non-spatial memory. Hippocampus 1: 258-261.
100. Rolls, E.T. 1992. Neurophysiological mechanisms underlying face processing within and beyond the temporal cortical visual areas. Philos. Trans. R. Soc. Lond. B Biol. Sci. 335: 11-21.
101. Rolls, E.T. 1994. Neurophysiological and neuronal network analysis of how the primate hippocampus functions in memory. In The memory system of the brain (ed. J. Delacour), pp. 713-744. World Scientific, London.
102. Rolls, E.T. 1995. A model of the operation of the hippocampus and entorhinal cortex in memory. Int. J. Neural Syst. 6: 51-70.
103. Rolls, E.T. 1996a. Roles of long term potentiation and long term depression in neuronal network operations in the brain. In Cortical plasticity (eds. M.S. Fazeli and G.L. Collingridge), pp. 223-250. Bios, Oxford.
104. Rolls, E.T. 1996b. A theory of hippocampal function in memory. Hippocampus 6: 601-620.
105. Rolls, E.T. 1999. Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9: 467-480.
106. Rolls, E.T. 2000. Memory systems in the brain. Annu. Rev. Psychol. 51: 599-630.
107. Rolls, E.T. 2003. Consciousness absent and present: A neurophysiological exploration. Prog. Brain Res. 144: 95-106.
108. Rolls, E.T. 2008. Memory, attention, and decision-making: A unifying computational neuroscience approach. Oxford University Press, Oxford.
109. Rolls, E.T. and Deco, G. 2002. Computational neuroscience of vision. Oxford University Press, Oxford.
110. Rolls, E.T. and Kesner, R.P. 2006. A computational theory of hippocampal function, and empirical tests of the theory. Prog. Neurobiol. 79: 1-48.
111. Rolls, E.T. and Stringer, S.M. 2005. Spatial view cells in the hippocampus, and their idiothetic update based on place and head direction. Neural Netw. 18: 1229-1241.
112. Rolls, E.T. and Treves, A. 1990. The relative advantages of sparse versus distributed encoding for associative neuronal networks in the brain. Network 1: 407-421.
113. Rolls, E.T. and Treves, A. 1998. Neural networks and brain function. Oxford University Press, Oxford.
114. Rolls, E.T. and Xiang, J.-Z. 2005. Reward-spatial view representations and learning in the hippocampus. J. Neurosci. 25: 6167-6174.
115. Rolls, E.T. and Xiang, J.-Z. 2006. Spatial view cells in the primate hippocampus, and memory recall. Rev. Neurosci. 17: 175-200.
116. Rolls, E.T., Miyashita, Y., Cahusac, P.M.B., Kesner, R.P., Niki, H., Feigenbaum, J., and Bach, L. 1989. Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown. J. Neurosci. 9: 1835-1845.
117. Rolls, E.T., Robertson, R.G., and Georges-François, P. 1997a. Spatial view cells in the primate hippocampus. Eur. J. Neurosci. 9: 1789-1794.
118. Rolls, E.T., Treves, A., Foster, D., and Perez-Vicente, C. 1997b. Simulation studies of the CA3 hippocampal subfield modelled as an attractor neural network. Neural Netw. 10: 1559-1569.
119. Rolls, E.T., Treves, A., Robertson, R.G., Georges-François, P., and Panzeri, S. 1998. Information about spatial view in an ensemble of primate hippocampal cells. J. Neurophysiol. 79: 1797-1813.
120. Rolls, E.T., Stringer, S.M., and Trappenberg, T.P. 2002. A unified model of spatial and episodic memory. Proc. R. Soc. Lond. B. Biol. Sci. 269: 1087-1093.
121. Rolls, E.T., Xiang, J.-Z., and Franco, L. 2005. Object, space and object-space representations in the primate hippocampus. J. Neurophysiol. 94: 833-844.
122. Rolls, E.T., Stringer, S.M., and Elliot, T. 2006. Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Network Comput. Neural Syst. 17: 447-465.
123. Rupniak, N.M.J. and Gaffan, D. 1987. Monkey hippocampus and learning about spatially directed movements. J. Neurosci. 7: 2331-2337.
124. Samsonovich, A. and McNaughton, B.L. 1997. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17: 5900-5920.
125. Schultz, S. and Rolls, E.T. 1999. Analysis of information transmission in the Schaffer collaterals. Hippocampus 9: 582-598.
126. Simmen, M.W., Treves, A., and Rolls, E.T. 1996. Pattern retrieval in threshold-linear associative nets. Network 7: 109-122.
127. Skaggs, W.E., Knierim, J.J., Kudrimoti, H.S., and McNaughton, B.L. 1995. A model of the neural basis of the rat's sense of direction. In Advances in neural information processing systems (eds. G. Tesauro et al.), pp. 173-180. MIT Press, Cambridge, MA.
128. Smith, M.L. and Milner, B. 1981. The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19: 781-793.
129. Stefanacci, L., Suzuki, W.A., and Amaral, D.G. 1996. Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys. J. Comp. Neurol. 375: 552-582.
130. Storm-Mathiesen, J., Zimmer, J., and Ottersen, O.P., eds. 1990. Understanding the brain through the hippocampus. Elsevier, Oxford.
131. Stringer, S.M. and Rolls, E.T. 2002. Invariant object recognition in the visual system with novel views of 3D objects. Neural Comput. 14: 2585-2596.
132. Stringer, S.M. and Rolls, E.T. 2006. Self-organizing path integration using a linked continuous attractor and competitive network: Path integration of head direction. Network Comput. Neural Syst. 17: 419-445.
133. Stringer, S.M., Rolls, E.T., Trappenberg, T.P., and de Araujo, I.E.T. 2002a. Self-organizing continuous attractor networks and path integration. Two-dimensional models of place cells. Network Comput. Neural Syst. 13: 429-446.
134. Stringer, S.M., Trappenberg, T.P., Rolls, E.T., and de Araujo, I.E.T. 2002b. Self-organizing continuous attractor networks and path integration: One-dimensional models of head direction cells. Network Comput. Neural Syst. 13: 217-242.
135. Stringer, S.M., Rolls, E.T., and Trappenberg, T.P. 2004. Self-organising continuous attractor networks with multiple activity packets, and the representation of space. Neural Netw. 17: 5-27.
136. Stringer, S.M., Rolls, E.T., and Trappenberg, T.P. 2005. Self-organizing continuous attractor network models of hippocampal spatial view cells. Neurobiol. Learn. Mem. 83: 79-92.
137. Sutherland, R.J. and Rudy, J.W. 1991. Exceptions to the rule of space. Hippocampus 1: 250-252.
138. Suzuki, W.A. and Amaral, D.G. 1994a. Perirhinal and parahippocampal cortices of the macaque monkey - Cortical afferents. J. Comp. Neurol. 350: 497-533.
139. Suzuki, W.A. and Amaral, D.G. 1994b. Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J. Neurosci. 14: 1856-1877.
140. Tabuchi, E., Mulder, A.B., and Wiener, S.I. 2003. Reward value invariant place responses and reward site associated activity in hippocampal neurons of behaving rats. Hippocampus 13: 117-132.
141. Taube, J.S., Muller, R.U., and Ranck, J.B.J. 1990. Head-direction cells recorded from the postsubiculum in freely moving rats. 1: Description and quantitative analysis. J. Neurosci. 10: 420-435.
142. Taube, J.S., Goodridge, J.P., Golob, E.J., Dudchenko, P.A., and Stackman, R.W. 1996. Processing the head direction signal: A review and commentary. Brain Res. Bull. 40: 477-486.
143. Taylor, J.G. 1999. Neural "bubble" dynamics in two dimensions: Foundations. Biol. Cybern. 80: 393-409.
144. Treves, A. 1990. Graded-response neurons and information encodings in autoassociative memories. Phys. Rev. A 42: 2418-2430.
145. Treves, A. 1993. Mean-field analysis of neuronal spike dynamics. Network 4: 259-284.
146. Treves, A. 1995. Quantitative estimate of the information relayed by Schaffer collaterals. J. Comput. Neurosci. 2: 259-272.
147. Treves, A. and Rolls, E.T. 1991. What determines the capacity of autoassociative memories in the brain? Network 2: 371-397.
148. Treves, A. and Rolls, E.T. 1992. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2: 189-199.
149. Treves, A. and Rolls, E.T. 1994. A computational analysis of the role of the hippocampus in memory. Hippocampus 4: 374-391.
150. van Haeften, T., Baks-te-Bulte, L., Goede, P.H., Wouterlood, F.G., and Witter, M.P. 2003. Morphological and numerical analysis of synaptic interactions between neurons in deep and superficial layers of the entorhinal cortex of the rat. Hippocampus 13: 943-952.
151. Van Hoesen, G.W. 1982. The parahippocampal gyrus. New observations regarding its cortical connections in the monkey. Trends Neurosci. 5: 345-350.
152. Wallace, D.G. and Whishaw, I.Q. 2003. NMDA lesions of Ammon's horn and the dentate gyrus disrupt the direct and temporally paced homing displayed by rats exploring a novel environment: Evidence for a role of the hippocampus in dead reckoning. Eur. J. Neurosci. 18: 513-523.
153. Whishaw, I.Q., Hines, D.J., and Wallace, D.G. 2001. Dead reckoning (path integration) requires the hippocampal formation: Evidence from spontaneous exploration and spatial learning tasks in light (allothetic) and dark (idiothetic) tests. Behav. Brain Res. 127: 49-69.
154. Witter, M.P. 1993. Organization of the entorhinal-hippocampal system: A review of current anatomical data. Hippocampus 3: 33-44.
155. Witter, M.P., Van Hoesen, G.W., and Amaral, D.G. 1989. Topographical organisation of the entorhinal projection to the dentate gyrus of the monkey. J. Neurosci. 9: 216-228.
156. Witter, M.P., Naber, P.A., van Haeften, T., Machielsen, W.C., Rombouts, S.A., Barkhof, F., Scheltens, P., and Lopes da Silva, F.H. 2000a. Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10: 398-410.
157. Witter, M.P., Wouterlood, F.G., Naber, P.A., and Van Haeften, T. 2000b. Anatomical organization of the parahippocampal-hippocampal network. Ann. N. Y. Acad. Sci. 911: 1-24.
158. Wood, E.R., Dudchenko, P.A., and Eichenbaum, H. 1999. The global record of memory in hippocampal neuronal activity. Nature 397: 613-616.
159. Zhang, K. 1996. Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: A theory. J. Neurosci. 16: 2112-2126.