The mechanisms for pattern completion and pattern separation in the hippocampus

Frontiers in Systems Neuroscience

Volumn 7, Issue OCT, 2013, Pages

  Rolls, Edmund T ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Attractor network; Competitive network; Episodic memory; Hippocampus; Pattern association network; Pattern completion; Pattern separation; Recall

Indexed keywords

BRAIN CORTEX; BRAIN FUNCTION; BRAIN NERVE CELL; COMPETITION; COMPETITIVE NETWORK; DENTATE GRANULE CELL; ENTORHINAL CORTEX; EPISODIC MEMORY; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL MOSSY FIBER; HUMAN; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY; NEOCORTEX; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PATTERN ASSOCIATION NETWORK; PATTERN COMPLETION; PATTERN SEPARATION; PRIMATE; RANDOMIZING EFFECT; RECALL; REVIEW; REWARD; RODENT; SYNAPSE; THEORY;

EID: 84887103754     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2013.00074     Document Type: Review

References (183)

1. Acsady, L., Kamondi, A., Sik, A., Freund, T., and Buzsaki, G. (1998). GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 18, 3386-3403.
2. Amaral, D. G. (1987). "Memory: anatomical organization of candidate brain regions, " inHandbook of Physiology. Section 1, The Nervous System, ed V. B. Mountcastle (Washington, DC: American Physiological Society), 211-294.
3. Amaral, D. G. (1993). Emerging principles of intrinsic hippocampal organisation. Curr. Opin. Neurobiol. 3, 225-229. doi: 10.1016/0959-4388(93)90214-J
4. Amaral, D. G., Ishizuka, N., and Claiborne, B. (1990). Neurons, numbers and the hippocampal network. Prog. Brain Res. 83, 1-11. doi: 10.1016/S0079-6123(08)61237-6
5. 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 (New York, NY: Wiley-Liss), 1-66.
6. 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. doi: 10.1016/0306-4522(89)90424-7
7. Amaral, D. G., and Witter, M. P. (1995). "The hippocampal formation, " in The Rat Nervous System, ed G. Paxinos (San Diego, CA: Academic Press), 443-493.
8. Amari, S. (1977). Dynamics of pattern formation in lateral-inhibition type neural fields. Biol. Cybern. 27, 77-87. doi: 10.1007/BF00337259
9. Amit, D. J. (1989). Modeling Brain Function. Cambridge: Cambridge University Press.
10. Amit, D. J., and Brunel, N. (1997). Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. Cereb. Cortex 7, 237-252. doi: 10.1093/cercor/7.3.237
11. Andersen, P., Morris, R. G. M., Amaral, D. G., Bliss, T. V. P., and O'Keefe, J. (2007). The Hippocampus Book. London: Oxford University Press.
12. Barkas, L. J., Henderson, J. L., Hamilton, D. A., Redhead, E. S., and Gray, W. P. (2010). Selective temporal resections and spatial memory impairment: cue dependent lateralization effects. Behav. Brain Res. 208, 535-544. doi: 10.1016/j.bbr.2009.12.035
13. Battaglia, F. P., and Treves, A. (1998). Attractor neural networks storing multiple space representations: a model for hippocampal place fields. Phys. Rev. E. 58, 7738-7753. doi: 10.1103/PhysRevE.58.7738
14. Bonelli, S. B., Powell, R. H., Yogarajah, M., Samson, R. S., Symms, M. R., Thompson, P. J., et al. (2010). Imaging memory in temporal lobe epilepsy: predicting the effects of temporal lobe resection. Brain 133, 1186-1199. doi: 10.1093/brain/awq006
15. 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. San Diego, CA: Academic Press.
16. Brown, T. H., Kairiss, E. W., and Keenan, C. L. (1990). Hebbian synapses: biophysical mechanisms and algorithms. Annu. Rev. Neurosci. 13, 475-511. doi: 10.1146/annurev.ne.13.030190.002355
17. Brun, V. H., Otnass, M. K., Molden, S., Steffenach, H. A., Witter, M. P., Moser, M. B., et al. (2002). Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296, 2243-2246. doi: 10.1126/science.1071089
18. 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. doi: 10.1002/cne.903460306
19. Cerasti, E., and Treves, A. (2010). How informative are spatial CA3 representations established by the dentate gyrus? PLoS Comput. Biol. 6:e1000759. doi: 10.1371/journal.pcbi.1000759
20. Cerasti, E., and Treves, A. (2013). The spatial representations acquired in CA3 by self-organizing recurrent connections. Front. Cell. Neurosci. 7:112. doi: 10.3389/fncel.2013.00112
21. Cheng, S. (2013). The CRISP theory of hippocampal function in episodic memory. Front. Neural Circuits 7:88. doi: 10.3389/fncir.2013.00088
22. Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D. Jr., Fragniere, A., Tyers, P., et al. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325, 210-213. doi: 10.1126/science.1173215
23. Daumas, S., Ceccom, J., Halley, H., Frances, B., and Lassalle, J. M. (2009). Activation of metabotropic glutamate receptor type 2/3 supports the involvement of the hippocampal mossy fiber pathway on contextual fear memory consolidation. Learn. Mem. 16, 504-507. doi: 10.1101/lm.1418309
24. Day, M., Langston, R., and Morris, R. G. (2003). Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 424, 205-209. doi: 10.1038/nature01769
25. 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. Hippocampus11, 699-706. doi: 10.1002/hipo.1085
26. Deco, G., Ledberg, A., Almeida, R., and Fuster, J. (2005). Neural dynamics of cross-modal and cross-temporal associations. Exp. Brain Res. 166, 325-336. doi: 10.1007/s00221-005-2374-y
27. Deco, G., and Rolls, E. T. (2003). Attention and working memory: a dynamical model of neuronal activity in the prefrontal cortex. Eur. J. Neurosci. 18, 2374-2390. doi: 10.1046/j.1460-9568.2003.02956.x
28. Deco, G., and Rolls, E. T. (2005). Sequential memory: a putative neural and synaptic dynamical mechanism. J. Cogn. Neurosci. 17, 294-307. doi: 10.1162/0898929053124875
29. Deco, G., and Rolls, E. T. (2006). Decision-making and Weber's Law: a neurophysiological model. Eur. J. Neurosci. 24, 901-916. doi: 10.1111/j.1460-9568.2006.04940.x
30. Deco, G., Rolls, E. T., Albantakis, L., and Romo, R. (2013). Brain mechanisms for perceptual and reward-related decision-making. Prog. Neurobiol. 103, 194-213. doi: 10.1016/j.pneurobio.2012.01.010
31. 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. doi: 10.1046/j.1460-9568.2002.01973.x
32. Dere, E., Easton, A., Nadel, L., and Huston, J. P. (eds.). (2008). Handbook of Episodic Memory. Amsterdam: Elsevier.
33. Faisal, A. A., Selen, L. P., and Wolpert, D. M. (2008). Noise in the nervous system. Nat. Rev. Neurosci. 9, 292-303. doi: 10.1038/nrn2258
34. Fazeli, M. S., and Collingridge, G. L. (eds.). (1996). Cortical Plasticity: LTP and LTD. Oxford: Bios.
35. 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. doi: 10.1016/j.bbr.2004.03.003
36. 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
37. 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. doi: 10.1126/science.1099901
38. 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. doi: 10.1093/cercor/9.3.197
39. Gilbert, P. E., and Kesner, R. P. (2003). Localization of function within the dorsal hippocampus: the role of the CA3 subregion in paired-associate learning. Behav. Neurosci. 117, 1385-1394. doi: 10.1037/0735-7044.117.6.1385
40. Gilbert, P. E., Kesner, R. P., and Lee, I. (2001). Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus 11, 626-636. doi: 10.1002/hipo.1077
41. Giocomo, L. M., and Hasselmo, M. E. (2007). Neuromodulation by glutamate and acetylcholine can change circuit dynamics by regulating the relative influence of afferent input and excitatory feedback. Mol. Neurobiol. 36, 184-200. doi: 10.1007/s12035-007-0032-z
42. Giocomo, L. M., Moser, M. B., and Moser, E. I. (2011). Computational models of grid cells. Neuron 71, 589-603. doi: 10.1016/j.neuron.2011.07.023
43. 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. doi: 10.1002/hipo.20103
44. Goodrich-Hunsaker, N. J., Hunsaker, M. R., and Kesner, R. P. (2008). The interactions and dissociations of the dorsal hippocampus subregions: how the dentate gyrus, CA3, and CA1 process spatial information. Behav. Neurosci. 122, 16-26. doi: 10.1037/0735-7044.122.1.16
45. 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. doi: 10.1038/nature03721
46. 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.
47. Henze, D. A., Wittner, L., and Buzsaki, G. (2002). Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat. Neurosci. 5, 790-795. doi: 10.1038/nn887
48. Hertz, J., Krogh, A., and Palmer, R. G. (1991). An Introduction to the Theory of Neural Computation. Wokingham: Addison-Wesley.
49. Hoge, J., and Kesner, R. P. (2007). Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects. Neurobiol. Learn. Mem. 88, 225-231. doi: 10.1016/j.nlm.2007.04.013
50. Hopfield, J. J. (1982). Neural networks and physical systems with emergent collective computational abilities. Proc. Natl. Acad. Sci. U.S.A. 79, 2554-2558. doi: 10.1073/pnas.79.8.2554
51. Hunsaker, M. R., and Kesner, R. P. (2008). Evaluating the differential roles of the dorsal dentate gyrus, dorsal CA3, and dorsal CA1 during a temporal ordering for spatial locations task. Hippocampus 18, 955-964. doi: 10.1002/hipo.20455
52. Hunsaker, M. R., and Kesner, R. P. (2013). The operation of pattern separation and pattern completion processes associated with different attributes or domains of memory. Neurosci. Biobehav. Rev. 37, 36-58. doi: 10.1016/j.neubiorev.2012.09.014
53. Hunsaker, M. R., Lee, B., and Kesner, R. P. (2008). Evaluating the temporal context of episodic memory: the role of CA3 and CA1. Behav. Brain Res. 188, 310-315. doi: 10.1016/j.bbr.2007.11.015
54. 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. doi: 10.1002/cne.902950407
55. Jackson, M. B. (2013). Recall of Spatial patterns stored in a hippocampal slice by long-term potentiation. J. Neurophysiol. doi: 10.1152/jn.00533.2013. [Epub ahead of print].
56. Jacobs, J., Weidemann, C. T., Miller, J. F., Solway, A., Burke, J. F., Wei, X. X., et al. (2013). Direct recordings of grid-like neuronal activity in human spatial navigation. Nat. Neurosci. 16, 1188-1190. doi: 10.1038/nn.3466
57. Jezek, K., Henriksen, E. J., Treves, A., Moser, E. I., and Moser, M.-B. (2011). Theta-paced flickering between place-cell maps in the hippocampus. Nature 278, 246-249. doi: 10.1038/nature10439
58. Jung, M. W., and McNaughton, B. L. (1993). Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3, 165-182. doi: 10.1002/hipo.450030209
59. Kesner, R. P. (2007). Behavioral functions of the CA3 subregion of the hippocampus. Learn. Mem. 14, 771-781. doi: 10.1101/lm.688207
60. Kesner, R. P. (2013). An analysis of the dentate gyrus function. Behav. Brain Res. 254, 1-7. doi: 10.1016/j.bbr.2013.01.012
61. Kesner, R. P., and Rolls, E. T. (2001). Role of long term synaptic modification in short term memory. Hippocampus 11, 240-250. doi: 10.1002/hipo.1040
62. Kesner, R. P., Gilbert, P. E., and Barua, L. A. (2002). The role of the hippocampus in memory for the temporal order of a sequence of odors. Behav. Neurosci. 116, 286-290. doi: 10.1037/0735-7044.116.2.286
63. Kesner, R. P., Hunsaker, M. R., and Warthen, M. W. (2008). The CA3 subregion of the hippocampus is critical for episodic memory processing by means of relational encoding in rats. Behav. Neurosci. 122, 1217-1225. doi: 10.1037/a0013592
64. Kesner, R. P., Morris, A. M., and Weeden, C. S. S. (2012). "Spatial, temporal, and associative behavioral functions associated with different subregions of the hippocampus, " in Oxford Handbook of Comparative Cognition, eds T. R. Zentall and E. A. Wasserman (Oxford: Oxford University Press), 322-346.
65. Killian, N. J., Jutras, M. J., and Buffalo, E. A. (2012). A map of visual space in the primate entorhinal cortex. Nature 491, 761-764. doi: 10.1038/nature11587
66. Kohonen, T. (1977). Associative Memory: A System Theoretical Approach. New York, NY: Springer. doi: 10.1007/978-3-642-96384-1
67. Kohonen, T. (1984). Self-Organization and Associative Memory. Berlin: Springer-Verlag.
68. Kohonen, T., Oja, E., and Lehtio, P. (1981). "Storage and processing of information in distributed memory systems, " in Parallel Models of Associative Memory, eds G. E. Hinton and J. A. Anderson (Hillsdale, NJ: Lawrence Erlbaum), 129-167.
69. Kondo, H., Lavenex, P., and Amaral, D. G. (2009). Intrinsic connections of the macaque monkey hippocampal formation: II. CA3 connections. J. Comp. Neurol. 515, 349-377. doi: 10.1002/cne.22056
70. Kropff, E., and Treves, A. (2008). The emergence of grid cells: intelligent design or just adaptation? Hippocampus 18, 1256-1269. doi: 10.1002/hipo.20520
71. 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. doi: 10.1006/nlme.1999.3931
72. Lavenex, P., and Amaral, D. G. (2000). Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10, 420-430. doi: 10.1002/1098-1063(2000)10:4<420::AID-HIPO8>3.3.CO;2-X
73. 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. doi: 10.1002/cne.20079
74. Lee, I., and Kesner, R. P. (2004). Encoding versus retrieval of spatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 14, 66-76. doi: 10.1002/hipo.10167
75. Lehn, H., Steffenach, H. A., Van Strien, N. M., Veltman, D. J., Witter, M. P., and Haberg, A. K. (2009). A specific role of the human hippocampus in recall of temporal sequences. J. Neurosci. 29, 3475-3484. doi: 10.1523/JNEUROSCI.5370-08.2009
76. Leutgeb, J. K., Leutgeb, S., Moser, M. B., and Moser, E. I. (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315, 961-966. doi: 10.1126/science.1135801
77. Leutgeb, S., and Leutgeb, J. K. (2007). Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map. Learn. Mem. 14, 745-757. doi: 10.1101/lm.703907
78. 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 (San Diego, CA: Academic Press), 243-305.
79. Lisman, J., and Redish, A. D. (2009). Prediction, sequences and the hippocampus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1193-1201. doi: 10.1098/rstb.2008.0316
80. Lynch, M. A. (2004). Long-term potentiation and memory. Physiol. Rev. 84, 87-136. doi: 10.1152/physrev.00014.2003
81. MacDonald, C. J., Lepage, K. Q., Eden, U. T., and Eichenbaum, H. (2011). Hippocampal "time cells" bridge the gap in memory for discontiguous events. Neuron 71, 737-749. doi: 10.1016/j.neuron.2011.07.012
82. Markov, N. T., Vezoli, J., Chameau, P., Falchier, A., Quilodran, R., Huissoud, C., et al. (2013). The anatomy of hierarchy: feedforward and feedback pathways in macaque visual cortex. J. Comp. Neurol. doi: 10.1002/cne.23458. [Epub ahead of print].
83. Marr, D. (1971). Simple memory: a theory for archicortex. Phil. Trans. Roy. Soc. Lond. B 262, 23-81. doi: 10.1098/rstb.1971.0078
84. 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. doi: 10.1037//0033-295X.102.3.419
85. McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., et al. (2007). Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317, 94-99. doi: 10.1126/science.1140263
86. McNaughton, B. L. (1991). Associative pattern completion in hippocampal circuits: new evidence and new questions. Brain Res. Rev. 16, 193-220.
87. 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. doi: 10.1007/BF00237147
88. 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. doi: 10.1038/nrn1932
89. 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. doi: 10.1016/0166-2236(87)90011-7
90. 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 (Hillsdale, NJ: Erlbaum), 1-64.
91. Miller, G. A. (1956). The magic number seven, plus or minus two: some limits on our capacity for the processing of information. Psychol. Rev. 63, 81-93. doi: 10.1037/h0043158
92. Miller, P., and Wang, X. J. (2006). Inhibitory control by an integral feedback signal in prefrontal cortex: a model of discrimination between sequential stimuli. Proc. Natl. Acad. Sci. U.S.A. 103, 201-206. doi: 10.1073/pnas.0508072103
93. Morris, R. G. (2003). Long-term potentiation and memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 643-647. doi: 10.1098/rstb.2002.1230
94. Morris, R. G., Moser, E. I., Riedel, G., Martin, S. J., Sandin, J., Day, M., et al. (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. doi: 10.1098/rstb.2002.1264
95. 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 (Oxford: Oxford University Press), 248-285.
96. Moscovitch, M., Rosenbaum, R. S., Gilboa, A., Addis, D. R., Westmacott, R., Grady, C., 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. doi: 10.1111/j.1469-7580.2005.00421.x
97. 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. doi: 10.1002/hipo.1028
98. Nakashiba, T., Cushman, J. D., Pelkey, K. A., Renaudineau, S., Buhl, D. L., McHugh, T. J., et al. (2012). Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149, 188-201. doi: 10.1016/j.cell.2012.01.046
99. Nakazawa, K., McHugh, T. J., Wilson, M. A., and Tonegawa, S. (2004). NMDA receptors, place cells and hippocampal spatial memory. Nat. Rev. Neurosci. 5, 361-372. doi: 10.1038/nrn1385
100. Nakazawa, K., Quirk, M. C., Chitwood, R. A., Watanabe, M., Yeckel, M. F., Sun, L. D., et al. (2002). Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297, 211-218. doi: 10.1126/science.1071795
101. Nakazawa, K., Sun, L. D., Quirk, M. C., Rondi-Reig, L., Wilson, M. A., and Tonegawa, S. (2003). Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38, 305-315. doi: 10.1016/S0896-6273(03)00165-X
102. O'Keefe, J. (1979). A review of the hippocampal place cells. Prog. Neurobiol. 13, 419-439. doi: 10.1016/0301-0082(79)90005-4
103. O'Keefe, J., and Nadel, L. (1978). The Hippocampus as a Cognitive Map. Oxford: Clarendon Press.
104. O'Keefe, J., and Speakman, A. (1987). Single unit activity in the rat hippocampus during a spatial memory task. Exp. Brain Res. 68, 1-27. doi: 10.1007/BF00255230
105. 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. doi: 10.1002/hipo.1099
106. Rajji, T., Chapman, D., Eichenbaum, H., and Greene, R. (2006). The role of CA3 hippocampal NMDA receptors in paired associate learning. J. Neurosci. 26, 908-915. doi: 10.1523/JNEUROSCI.4194-05.2006
107. 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.
108. 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 (Chichester: Wiley), 503-540.
109. 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 (Cambridge: Cambridge University Press), 15-33.
110. 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 (San Diego, CA: Academic Press), 240-265.
111. 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, C. Miall G. Mitchison (Wokingham, England: Addison-Wesley), 125-159.
112. 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 (Hillsdale, NJ: L. Erlbaum), 339-362.
113. 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. doi: 10.1101/SQB.1990.055.01.095
114. Rolls, E. T. (1991). Functions of the primate hippocampus in spatial and non-spatial memory. Hippocampus 1, 258-261. doi: 10.1002/hipo.450010310
115. Rolls, E. T. (1995). A model of the operation of the hippocampus and entorhinal cortex in memory. Int. J. Neural Syst. 6, 51-70.
116. 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 (Oxford: Bios), 223-250.
117. Rolls, E. T. (1996b). A theory of hippocampal function in memory. Hippocampus 6, 601-620. doi: 10.1002/(SICI)1098-1063(1996)6:6<601::AID-HIPO5>3.0.CO;2-J
118. Rolls, E. T. (1999). Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9, 467-480. doi: 10.1002/(SICI)1098-1063(1999)9:4<467::AID-HIPO13>3.3.CO;2-6
119. Rolls, E. T. (2008). Memory, Attention, and Decision-Making: A Unifying Computational Neuroscience Approach. Oxford: Oxford University Press.
120. Rolls, E. T. (2010a). Attractor networks. WIRE Cogn. Sci. 1, 119-134. doi: 10.1002/wcs.1
121. Rolls, E. T. (2010b). A computational theory of episodic memory formation in the hippocampus. Behav. Brain Res. 205, 180-196. doi: 10.1016/j.bbr.2010.03.027
122. Rolls, E. T. (2012a). Advantages of dilution in the connectivity of attractor networks in the brain. Biol. Inspired Cogn. Archit. 1, 44-54. doi: 10.1016/j.bica.2012.03.003
123. Rolls, E. T. (2012b). Invariant visual object and face recognition: neural and computational bases, and a model, VisNet. Front. Comput. Neurosci. 6:35. doi: 10.3389/fncom.2012.00035
124. Rolls, E. T. (2013). A quantitative theory of the functions of the hippocampal CA3 network in memory. Front. Cell Neurosci. 7:98. doi: 10.3389/fncel.2013.00098
125. Rolls, E. T. (2014a). Emotion and Decision-Making Explained. Oxford: Oxford University Press.
126. Rolls, E. T. (2014b). Limbic systems for emotion and for memory, but no single limbic system. Cortex.
127. Rolls, E. T., and Deco, G. (2002). Computational Neuroscience of Vision. Oxford: Oxford University Press.
128. Rolls, E. T., and Deco, G. (2010). The Noisy Brain: Stochastic Dynamics as a Principle of Brain Function. Oxford: Oxford University Press. doi: 10.1093/acprof:oso/9780199587865.001.0001
129. Rolls, E. T., Dempere-Marco, L., and Deco, G. (2013). Holding multiple items in short term memory: a neural mechanism. PLoS ONE 8:e61078. doi: 10.1371/journal.pone.0061078
130. 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. doi: 10.1016/j.pneurobio.2006.04.005
131. Rolls, E. T., Robertson, R. G., and Georges-François, P. (1997a). Spatial view cells in the primate hippocampus. Eur. J. Neurosci. 9, 1789-1794. doi: 10.1111/j.1460-9568.1997.tb01538.x
132. 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. doi: 10.1016/S0893-6080(97)00092-0
133. Rolls, E. T., and Stringer, S. M. (2000). On the design of neural networks in the brain by genetic evolution. Prog. Neurobiol. 61, 557-579. doi: 10.1016/S0301-0082(99)00066-0
134. 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. doi: 10.1016/j.neunet.2005.08.006
135. Rolls, E. T., Stringer, S. M., and Elliot, T. (2006). Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Network 17, 447-465. doi: 10.1080/09548980601064846
136. Rolls, E. T., Stringer, S. M., and Trappenberg, T. P. (2002). A unified model of spatial and episodic memory. Proc. R. Soc. Lond. B 269, 1087-1093. doi: 10.1098/rspb.2002.2009
137. 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. doi: 10.1088/0954-898X/1/4/002
138. 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.
139. Rolls, E. T., and Treves, A. (1998). Neural Networks and Brain Function. Oxford: Oxford University Press.
140. Rolls, E. T., and Treves, A. (2011). The neuronal encoding of information in the brain. Prog. Neurobiol. 95, 448-490. doi: 10.1016/j.pneurobio.2011.08.002
141. Rolls, E. T., and Webb, T. J. (2012). Cortical attractor network dynamics with diluted connectivity. Brain Res. 1434, 212-225. doi: 10.1016/j.brainres.2011.08.002
142. Rolls, E. T., and Xiang, J.-Z. (2005). Reward-spatial view representations and learning in the hippocampus. J. Neurosci. 25, 6167-6174. doi: 10.1523/JNEUROSCI.1481-05.2005
143. Rolls, E. T., and Xiang, J.-Z. (2006). Spatial view cells in the primate hippocampus, and memory recall. Rev. Neurosci. 17, 175-200. doi: 10.1515/REVNEURO.2006.17.1-2.175
144. 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. doi: 10.1152/jn.01063.2004
145. Rondi-Reig, L., Libbey, M., Eichenbaum, H., and Tonegawa, S. (2001). CA1-specific N-methyl-D-aspartate receptor knockout mice are deficient in solving a nonspatial transverse patterning task. Proc. Natl. Acad. Sci. U.S.A. 98, 3543-3548. doi: 10.1073/pnas.041620798
146. Samsonovich, A., and McNaughton, B. L. (1997). Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900-5920.
147. Schultz, S., Panzeri, S., Rolls, E. T., and Treves, A. (2000). "Chap. 14. Quantitive model analysis of a Schaffer collateral model, " in Information Theory and the Brain, ed P. Hancock, P. Foldiak and R. Baddeley (Cambridge: Cambridge University Press), 257-272.
148. Schultz, S., and Rolls, E. T. (1999). Analysis of information transmission in the Schaffer collaterals. Hippocampus 9, 582-598. doi: 10.1002/(SICI)1098-1063(1999)9:5<582::AID-HIPO12>3.0.CO;2-P
149. Schwindel, C. D., and McNaughton, B. L. (2011). Hippocampal-cortical interactions and the dynamics of memory trace reactivation. Prog. Brain Res. 193, 163-177. doi: 10.1016/B978-0-444-53839-0.00011-9
150. Sidhu, M. K., Stretton, J., Winston, G. P., Bonelli, S., Centeno, M., Vollmar, C., et al. (2013). A functional magnetic resonance imaging study mapping the episodic memory encoding network in temporal lobe epilepsy. Brain 136, 1868-1888. doi: 10.1093/brain/awt099
151. Simmen, M. W., Treves, A., and Rolls, E. T. (1996). Pattern retrieval in threshold-linear associative nets. Network 7, 109-122. doi: 10.1088/0954-898X/7/1/007
152. 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. doi: 10.1002/(SICI)1096-9861(19961125)375:4<552::AID-CNE2>3.3.CO;2-J
153. Stella, F., Cerasti, E., and Treves, A. (2013). Unveiling the metric structure of internal representations of space. Front. Neural Circuits 7:81. doi: 10.3389/fncir.2013.00081
154. Storm-Mathiesen, J., Zimmer, J., and Ottersen, O. P. (eds.). (1990). Understanding the Brain Through the Hippocampus. Oxford: Elsevier.
155. 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. doi: 10.1162/089976602760407982
156. 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. Network17, 419-445. doi: 10.1080/09548980601004032
157. 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 Networks 17, 5-27. doi: 10.1016/S0893-6080(03)00210-7
158. 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. doi: 10.1016/j.nlm.2004.08.003
159. Stringer, S. M., Rolls, E. T., Trappenberg, T. P., and Araujo, I. E. T. (2002a). Self-organizing continuous attractor networks and path integration. Two-dimensional models of place cells. Network 13, 429-446. doi: 10.1088/0954-898X/13/4/301
160. Stringer, S. M., Trappenberg, T. P., Rolls, E. T., and Araujo, I. E. T. (2002b). Self-organizing continuous attractor networks and path integration: one-dimensional models of head direction cells. Network 13, 217-242. doi: 10.1088/0954-898X/13/2/304
161. Suzuki, W. A., and Amaral, D. G. (1994a). Perirhinal and parahippocampal cortices of the macaque monkey-cortical afferents. J. Comp. Neurol. 350, 497-533. doi: 10.1002/cne.903500402
162. 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.
163. Taylor, J. G. (1999). Neural "bubble" dynamics in two dimensions: foundations. Biol. Cybern. 80, 393-409. doi: 10.1007/s004220050534
164. Tonegawa, S., Nakazawa, K., and Wilson, M. A. (2003). Genetic neuroscience of mammalian learning and memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 787-795. doi: 10.1098/rstb.2002.1243
165. Treves, A. (1990). Graded-response neurons and information encodings in autoassociative memories. Phys. Rev. A 42, 2418-2430. doi: 10.1103/PhysRevA.42.2418
166. Treves, A. (1991). Dilution and sparse coding in threshold-linear nets. J. Phys. A 24, 327-335. doi: 10.1088/0305-4470/24/1/038
167. Treves, A. (1995). Quantitative estimate of the information relayed by Schaffer collaterals. J. Comput. Neurosci. 2, 259-272. doi: 10.1007/BF00961437
168. Treves, A., and Rolls, E. T. (1991). What determines the capacity of autoassociative memories in the brain? Network 2, 371-397. doi: 10.1088/0954-898X/2/4/004
169. 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. doi: 10.1002/hipo.450020209
170. Treves, A., and Rolls, E. T. (1994). A computational analysis of the role of the hippocampus in memory. Hippocampus 4, 374-391. doi: 10.1002/hipo.450040319
171. 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. doi: 10.1002/hipo.10144
172. Van Hoesen, G. W. (1982). The parahippocampal gyrus. New observations regarding its cortical connections in the monkey. Trends Neurosci. 5, 345-350. doi: 10.1016/0166-2236(82)90201-6
173. Walters, D. M., Stringer, S. M., and Rolls, E. T. (2013). Path integration of head direction: updating a packet of neural activity at the correct speed using axonal conduction delays. PLoS ONE 8:e58330. doi: 10.1371/journal.pone.0058330
174. Wang, S. H., and Morris, R. G. (2010). Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu. Rev. Psychol. 61, 49-79, C41-C44. doi: 10.1146/annurev.psych.093008.100523
175. Wang, X. J. (2002). Probabilistic decision making by slow reverberation in cortical circuits. Neuron 36, 955-968. doi: 10.1016/S0896-6273(02)01092-9
176. Webb, T., Rolls, E. T., Deco, G., and Feng, J. (2011). Noise in attractor networks in the brain produced by graded firing rate representations. PLoS ONE 6:e23630. doi: 10.1371/journal.pone.0023630
177. Wills, T. J., Lever, C., Cacucci, F., Burgess, N., and O'Keefe, J. (2005). Attractor dynamics in the hippocampal representation of the local environment. Science 308, 873-876. doi: 10.1126/science.1108905
178. Witter, M. P. (1993). Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus 3, 33-44.
179. Witter, M. P. (2007). Intrinsic and extrinsic wiring of CA3: indications for connectional heterogeneity. Learn. Mem. 14, 705-713. doi: 10.1101/lm.725207
180. Witter, M. P., Naber, P. A., Van Haeften, T., Machielsen, W. C., Rombouts, S. A., Barkhof, F., et al. (2000a). Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10, 398-410. doi: 10.1002/1098-1063(2000)10:4<398::AID-HIPO6>3.3.CO;2-B
181. 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. doi: 10.1111/j.1749-6632.2000.tb06716.x
182. Zhang, K. (1996). Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J. Neurosci. 16, 2112-2126.
183. Zilli, E. A. (2012). Models of grid cell spatial firing published 2005-2011. Front. Neural Circuits 6:16. doi: 10.3389/fncir.2012.00016