Complementary learning systems

Cognitive Science

Volumn 38, Issue 6, 2014, Pages 1229-1248

  O'Reilly, Randall C ^a   Bhattacharyya, Rajan ^b   Howard, Michael D ^b   Ketz, Nicholas ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b Hughes Aircraft Co   (United States)

Author keywords

Consolidation; Hippocampus; Learning; Memory; Neocortex; Neural network models

Indexed keywords

BIOLOGICAL MODEL; EPISODIC MEMORY; HIPPOCAMPUS; HUMAN; LEARNING; NEOCORTEX; NERVE TRACT; PHYSIOLOGY; RECOGNITION;

HIPPOCAMPUS; HUMANS; LEARNING; MEMORY, EPISODIC; MODELS, NEUROLOGICAL; NEOCORTEX; NEURAL PATHWAYS; RECOGNITION (PSYCHOLOGY);

EID: 84906085462     PISSN: 03640213     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1551-6709.2011.01214.x     Document Type: Article

References (89)

1. Aisa, B., Mingus, B., & O'Reilly, R. ( 2008 ). The emergent neural modeling system . Neural Networks, 21 ( 8 ), 1146 - 1152 .
2. Bakker, A., Kirwan, B. C., Miller, M., & Stark, C. E. ( 2008 ). Pattern separation in the human hippocampal CA3 and dentate gyrus . Science, 319 ( 5870 ), 1640 - 1642 .
3. Barense, M. D., Bussey, T. J., Lee, A. C. H., Rogers, T. T., Davies, R. R., Saksida, L. M., Murray, E. A., & Graham, K. S. ( 2005 ). Functional specialization in the human medial temporal lobe . The Journal of Neuroscience, 25 ( 44 ), 10239 - 10246 .
4. Barnes, J. M., & Underwood, B. J. ( 1960 ). Fate of first-list associations in transfer theory . Journal of Experimental Psychology, 58, 97 - 105 .
5. Blumenfeld, R. S., & Ranganath, C. ( 2007 ). Prefrontal cortex and long-term memory encoding: An integrative review of findings from neuropsychology and neuroimaging . The Neuroscientist, 13 ( 3 ), 280 - 291 .
6. Braver, T. S., Barch, D. M., Keys, B. A., Carter, C. S., Cohen, J. D., Kaye, J. A., Janowsky, J. S., Taylor, S. F., Yesavage, J. A., Mumenthaler, M. S., Jagust, W. J., & Reed, B. R. ( 2001 ). Context processing in older adults: Evidence for a theory relating cognitive control to neurobiology in healthy aging . Journal of Experimental Psychology: General, 130, 746 - 763 .
7. Buzsaki, G. ( 2002 ). Theta oscillations in the hippocampus . Neuron, 33 ( 3 ), 325 - 340 .
8. Chatham, C. H., Frank, M. J., & Munakata, Y. ( 2009 ). Pupillometric and behavioral markers of a developmental shift in the temporal dynamics of cognitive control . Proceedings of the National Academy of Sciences of the United States of America, 106 ( 14 ), 5529 - 5533 .
9. Clelland, C., Choi, M., Romberg, C., Clemenson, G., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L., Barker, R., Gage, F., & Bussey, T. ( 2009 ). A functional role for adult hippocampal neurogenesis in spatial pattern separation . Science, 325, 210 - 213 .
10. Colgin, L. L., Denninger, T., Fyhn, M., Hafting, T., Bonnevie, T., Jensen, O., Moser, M.-B., & Moser, E. I. ( 2009 ). Frequency of gamma oscillations routes flow of information in the hippocampus . Nature, 462 ( 7271 ), 353 - 357 .
11. Cowell, R. A., Bussey, T. J., & Saksida, L. M. ( 2010 ). Components of recognition memory: Dissociable cognitive processes or just differences in representational complexity?Hippocampus, 20, 1245 - 1262 .
12. Dusek, J. A., & Eichenbaum, H. ( 1997 ). The hippocampus and memory for orderly stimulus relations . Proceedings of the National Academy of Sciences of the United States of America, 94, 7109 - 7114 .
13. Elfman, K. W., Parks, C. M., & Yonelinas, A. P. ( 2008 ). Testing a neurocomputational model of recollection, familiarity, and source recognition . Journal of Experimental Psychology, 34 ( 4 ), 752 - 768 .
14. Eschenko, O., Ramadan, W., Molle, M., Born, J., & Sara, S. J. ( 2008 ). Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning . Learning & Memory, 15 ( 4 ), 222 - 228 .
15. Euston, D. R., & McNaughton, B. L. ( 2006 ). Apparent encoding of sequential context in rat medial prefrontal cortex is accounted for by behavioral variability . The Journal of Neuroscience, 26 ( 51 ), 13143 - 13155 .
16. Frank, M. J., Rudy, J. W., & O'Reilly, R. C. ( 2003 ). Transitivity, flexibility, conjunctive representations and the hippocampus. II. A computational analysis . Hippocampus, 13, 341 - 354 .
17. Gilbert, P. E., Kesner, R. P., & Lee, I. ( 2001 ). Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1 . Hippocampus, 11, 626 - 636 .
18. Girardeau, G., Benchenane, K., Wiener, S. I., Buzsaki, G., & Zugaro, M. B. ( 2009 ). Selective suppression of hippocampal ripples impairs spatial memory . Nature Neuroscience, 12 ( 10 ), 1222 - 1223 .
19. Hafting, T., Fyhn, M., Bonnevie, T., Moser, M.-B., & Moser, E. I. ( 2008 ). Hippocampus-independent phase precession in entorhinal grid cells . Nature, 453 ( 7199 ), 1248 - 1252 .
20. Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. ( 2005 ). Microstructure of a spatial map in the entorhinal cortex . Nature, 436, 801 - 806 .
21. Hasselmo, M. E. ( 1999 ). Neuromodulation: Acetylcholine and memory consolidation . Trends in Cognitive Sciences, 3 ( 9 ), 351 - 359 .
22. Hasselmo, M. E., Bodelon, C., & Wyble, B. P. ( 2002 ). A proposed function for hippocampal theta rhythm: Separate phases of encoding and retrieval enhance reversal of prior learning . Neural Computation, 14, 793 - 818 .
23. Hasselmo, M. E., Schnell, E., & Barkai, E. ( 1995 ). Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3 . Journal of Neuroscience, 15 ( 7 Pt 2 ), 5249 - 5262 .
24. Hasselmo, M. E., & Stern, C. E. ( 2006 ). Mechanisms underlying working memory for novel information . Trends in Cognitive Sciences, 10 ( 11 ), 487 - 493 .
25. Hinton, G. E., McClelland, J. L., & Rumelhart, D. E. ( 1986 ). Distributed representations . In D. E.Rumelhart, J. L.McClelland, & P. R.Group ( Eds .), Parallel distributed processing. Volume 1: Foundations ( Chapter 3, pp . 77 - 109 ). Cambridge, MA: MIT Press .
26. Hintzman, D. L. ( 1988 ). Judgments of frequency and recognition memory in a multiple-trace memory model . Psychological Review, 95, 528 - 551 .
27. Ji, D., & Wilson, M. A. ( 2007 ). Coordinated memory replay in the visual cortex and hippocampus during sleep . Nature Neuroscience, 10 ( 1 ), 100 - 107 .
28. Jones, M. W., & Wilson, M. A. ( 2005 ). Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task . PLoS Biology, 3, e402 .
29. Karlsson, M. P., & Frank, L. M. ( 2009 ). Awake replay of remote experiences in the hippocampus . Nature Neuroscience, 12 ( 7 ), 913 - 918 .
30. Kumaran, D., & McClelland, J. ( 2010, November ). Generalization through recurrence: An interactive model of the hippocampus . Poster presented at the Annual Meeting of the Society for Neuroscience, San Diego, CA .
31. Lee, A. K., & Wilson, M. A. ( 2002 ). Memory of sequential experience in the hippocampus during slow wave sleep . Neuron, 36, 1183 - 1194 .
32. Leutgeb, J. K., Leutgeb, S., Moser, M., & Moser, E. ( 2007 ). Pattern separation in the dentate gyrus and CA3 of the hippocampus . Science, 315 ( 5814 ), 961 - 966 .
33. Louie, K., & Wilson, M. ( 2001 ). Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep . Neuron, 29, 145 - 146 .
34. Manns, J. R., Zilli, E. A., Ong, K. C., Hasselmo, M. E., & Eichenbaum, H. ( 2007 ). Hippocampal CA1 spiking during encoding and retrieval: Relation to theta phase . Neurobiology of Learning and Memory, 87 ( 1 ), 9 - 20 .
35. Marr, D. ( 1972 ). Simple memory: A theory for archicortex . Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 262, 23 - 81 .
36. McClelland, J. L. ( 2000 ). The basis of hyperspecificity in autism: A preliminary suggestion based on properties of neural nets . Journal of Autism and Developmental Disorders, 30, 497 - 502 .
37. McClelland, J. L., & Goddard, N. H. ( 1997 ). Considerations arising from a complementary learning systems perspective on hippocampus and neocortex . Hippocampus, 6, 654 - 665 .
38. 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, 419 - 457 .
39. McClelland, J. L., & Rumelhart, D. E. ( 1986 ). A distributed model of human learning and memory . In J. L.McClelland, D. E.Rumelhart, & P. R.Group ( Eds .), Parallel distributed processing. Volume 2: Psychological and biological models ( pp . 170 - 215 ). Cambridge, MA: MIT Press .
40. McCloskey, M., & Cohen, N. J. ( 1989 ). Catastrophic interference in connectionist networks: The sequential learning problem . In G. H.Bower ( Ed .), The psychology of learning and motivation, vol. 24 ( pp . 109 - 164 ). San Diego, CA: Academic Press .
41. McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., Lowell, B. B., Fanselow, M. S., Wilson, M. A., & Tonegawa, S. ( 2007 ). Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network . Science, 317 ( 5834 ), 94 - 99 .
42. McNaughton, B. L., & Morris, R. G. M. ( 1987 ). Hippocampal synaptic enhancement and information storage within a distributed memory system . Trends in Neurosciences, 10 ( 10 ), 408 - 415 .
43. Molyneaux, B. J., & Hasselmo, M. E. ( 2002 ). Gabab presynaptic inhibition has an in vivo time constant sufficiently rapid to allow modulation at theta frequency . Journal of Neurophysiology, 87 ( 3 ), 1196 - 1205 .
44. Nadasdy, Z., Hirase, H., Czurko, A., Csicsvari, J., & Buzsaki, G. ( 1999 ). Replay and time compression of recurring spike sequences in the hippocampus . The Journal of Neuroscience, 19 ( 21 ), 9497 - 9507 .
45. Nadel, L., & Moscovitch, M. ( 1997 ). Memory consolidation, retrograde amnesia and the hippocampal complex . Current Opinion in Neurobiology, 7, 217 .
46. Nakashiba, T., Young, J. Z., McHugh, T. J., Buhl, D. L., & Tonegawa, S. ( 2008 ). Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning . Science, 319 ( 5867 ), 1260 - 1264 .
47. Norman, K. A. ( 2010 ). How hippocampus and cortex contribute to recognition memory: Revisiting the complementary learning systems model . Hippocampus, 20, 1217 - 1227 .
48. Norman, K. A., Newman, E. L., & Detre, G. ( 2007 ). A neural network model of retrieval-induced forgetting . Psychological Review, 114 ( 4 ), 887 - 953 .
49. Norman, K. A., Newman, E., Detre, G., & Polyn, S. ( 2006 ). How inhibitory oscillations can train neural networks and punish competitors . Neural Computation, 18 ( 7 ), 1577 - 610 .
50. Norman, K. A., Newman, E. L., & Perotte, A. J. ( 2005 ). Methods for reducing interference in the complementary learning systems model: Oscillating inhibition and autonomous memory rehearsal . Neural Networks, 18 ( 9 ), 1212 - 1228 .
51. Norman, K. A., & O'Reilly, R. C. ( 2003 ). Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning-systems approach . Psychological Review, 110, 611 - 646 .
52. O'Mara, S. M., Sanchez-Vives, M. V., Brotons-Mas, J. R., & O'Hare, E. ( 2009 ). Roles for the subiculum in spatial information processing, memory, motivation and the temporal control of behaviour . Progress in Neuro-Psychopharmacology & Biological Psychiatry, 33, 782 - 790 .
53. O'Reilly, R. C. ( 1996 ). Biologically plausible error-driven learning using local activation differences: The generalized recirculation algorithm . Neural Computation, 8 ( 5 ), 895 - 938 .
54. O'Reilly, R. C. ( 1998 ). Six principles for biologically-based computational models of cortical cognition . Trends in Cognitive Sciences, 2 ( 11 ), 455 - 462 .
55. O'Reilly, R. C. ( 2001 ). Generalization in interactive networks: The benefits of inhibitory competition and Hebbian learning . Neural Computation, 13, 1199 - 1242 .
56. O'Reilly, R. C., & McClelland, J. L. ( 1994 ). Hippocampal conjunctive encoding, storage, and recall: Avoiding a tradeoff . Hippocampus, 4 ( 6 ), 661 - 682 .
57. O'Reilly, R. C., & Munakata, Y. ( 2000 ). Computational explorations in cognitive neuroscience: Understanding the mind by simulating the brain . Cambridge, MA: The MIT Press .
58. O'Reilly, R. C., & Rudy, J. W. ( 2001 ). Conjunctive representations in learning and memory: Principles of cortical and hippocampal function . Psychological Review, 108, 311 - 345 .
59. Peigneux, P., Laureys, S., Fuchs, S., Collette, F., Perrin, F., Reggers, J., Phillips, C., Degueldre, C., Fiore, G., Aerts, J., Luxen, A., & Maquet, P. ( 2004 ). Are spatial memories strengthened in the human hippocampus during slow wave sleep?Neuron, 44, 535 - 545 .
60. Peyrache, A., Khamassi, M., Benchenane, K., Wiener, S. I., & Battaglia, F. P. ( 2009 ). Replay of rule-learning related neural patterns in the prefrontal cortex during sleep . Nature Neuroscience, 12 ( 7 ), 919 - 926 .
61. Qin, Y. L., McNaughton, B. L., Skaggs, W. E., & Barnes, C. A. ( 1997 ). Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles . Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 352 ( 1360 ), 1525 - 1533 .
62. Rasch, B., & Born, J. ( 2007 ). Maintaining memories by reactivation . Current Opinion in Neurobiology, 17 ( 6 ), 698 - 703 .
63. Reynolds, J. R., Braver, T. S., Brown, J. W., & van der Stigchel, S. ( 2006 ). Computational and neural mechanisms of task switching . Neurocomputing, 69, 1332 - 1336 .
64. Rizzuto, D. S., Madsen, J. R., Bromfield, E. B., Schulze-Bonhage, A., Seelig, D., Aschenbrenner-Scheibe, R., & Kahana, M. J. ( 2003 ). Reset of human neocortical oscillations during a working memory task . Proceedings of the National Academy of Sciences of the United States of America, 100, 7931 - 7936 .
65. Robins, A., & McCallum, S. ( 1999 ). The consolidation of learning during sleep: Comparing the pseudorehearsal and unlearning accounts . Neural Networks, 12 ( 7-8 ), 1191 - 1206 .
66. Rolls, E. T. ( 1989 ). Functions of neuronal networks in the hippocampus and neocortex in memory . In J. H.Byrne & W. O.Berry ( Eds .), Neural models of plasticity: Experimental and theoretical approaches ( pp . 240 - 265 ). San Diego, CA: Academic Press .
67. Rudy, J. W., & O'Reilly, R. C. ( 1999 ). Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus . Behavioral Neuroscience, 113, 867 - 880 .
68. Rudy, J. W., & Sutherland, R. J. ( 1996 ). Configural association theory and the hippocampal formation: An appraisal and reconfiguration . Hippocampus, 5, 375 - 389 .
69. Sherry, D. F., & Schacter, D. L. ( 1987 ). The evolution of multiple memory systems . Psychological Review, 94 ( 4 ), 439 - 454 .
70. Shimamura, A. P. ( 2010 ). Hierarchical relational binding in the medial temporal lobe: The strong get stronger . Hippocampus, 20, 1206 - 1216 .
71. Shimamura, A. P., & Wickens, T. D. ( 2009 ). Superadditive memory strength for item and source recognition: The role of hierarchical relational binding in the medial temporal lobe . Psychological Review, 116 ( 1 ), 1 - 19 .
72. Siapas, A., & Wilson, M. ( 1998 ). Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep . Neuron, 21 ( 21 ), 1123 - 1128 .
73. Skaggs, W. E., McNaughton, B. L., Permenter, M., Archibeque, M., Vogt, J., Amaral, D. G., & Barnes, C. A. ( 2007 ). EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus . Journal of Neurophysiology, 98 ( 2 ), 898 - 910 .
74. Stickgold, R. ( 2005 ). Sleep-dependent memory consolidation . Nature, 437, 1272 - 1278 .
75. Susanne, D., & Jan, B. ( 2010 ). The memory function of sleep . Nature Reviews, 11 ( 2 ), 114 - 126 .
76. Sutherland, R. J., O'Brien, J., & Lehmann, H. ( 2008 ). Absence of systems consolidation of fear memories after dorsal, ventral, or complete hippocampal damage . Hippocampus, 18 ( 7 ), 710 - 718 .
77. Sutherland, R. J., & Rudy, J. W. ( 1989 ). Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia . Psychobiology, 17 ( 2 ), 129 - 144 .
78. Tambini, A., Ketz, N., & Davachi, L. ( 2010 ). Enhanced brain correlations during rest are related to memory for recent experiences . Neuron, 65 ( 2 ), 280 - 290 .
79. Viard, A., Lebreton, K., Chetelat, G., Desgranges, B., Landeau, B., Young, A., De La Sayette, V., Eustache, F., & Piolino, P. ( 2010 ). Patterns of hippocampal-neocortical interactions in the retrieval of episodic autobiographical memories across the entire life-span of aged adults . Hippocampus, 20 ( 1 ), 153 - 165 .
80. Voss, J. L., & Paller, K. A. ( 2010 ). Bridging divergent neural models of recognition memory: Introduction to the special issue and commentary on key issues . Hippocampus, 20 ( 11 ), 1171 - 1177 .
81. Wilson, M. A., & McNaughton, B. L. ( 1994 ). Reactivation of hippocampal ensemble memories during sleep . Science, 265, 676 - 678 .
82. Winocur, G., Moscovitch, M., & Bontempi, B. ( 2010 ). Memory formation and long-term retention in humans and animals: Convergence towards a transformation account of hippocampal-neocortical interactions . Neuropsychologia, 48, 2339 - 2356 .
83. Winters, B. D., Saksida, L. M., & Bussey, T. J. ( 2008 ). Object recognition memory: Neurobiological mechanisms of encoding, consolidation and retrieval . Neuroscience and Biobehavioral Reviews, 32, 1055 - 1070 .
84. Wixted, J. T., Mickes, L., & Squire, L. R. ( 2010 ). Measuring recollection and familiarity in the medial temporal lobe . Hippocampus, 20, 1195 - 1205 .
85. Wyble, B. P., Linster, C., & Hasselmo, M. E. ( 2000 ). Size of CA1-evoked synaptic potentials is related to theta rhythm phase in rat hippocampus . Journal of Neurophysiology, 83 ( 4 ), 2138 - 2144 .
86. Yonelinas, A. P. ( 2002 ). The nature of recollection and familiarity: A review of 30years of research . Journal of Memory and Language, 46, 441 - 517 .
87. Yonelinas, A. P., Aly, M., Wang, W.-C., & Koen, J. D. ( 2010 ). Recollection and familiarity: Examining controversial assumptions and new directions . Hippocampus, 20, 1178 - 1194 .
88. Yonelinas, A. P., Dobbins, I., Szymanski, M. D., Dhaliwal, H. S., & King, L. ( 1997 ). Signal-detection, threshold, and dual-process models of recognition memory: Rocs and conscious recollection . Consciousness and Cognition, 5, 418 - 441 .
89. Yotsumoto, Y., Kahana, M. J., Wilson, H. R., & Sekuler, R. ( 2007 ). Recognition memory for realistic synthetic faces . Memory and Cognition, 35 ( 6 ), 1233 - 1244 .