A phase code for memory could arise from circuit mechanisms in entorhinal cortex

Neural Networks

Volumn 22, Issue 8, 2009, Pages 1129-1138

  Hasselmo, Michael E ^a   Brandon, Mark P ^a   Yoshida, Motoharu ^a   Giocomo, Lisa M ^a   Heys, James G ^a   Fransen, Erik ^a   Newman, Ehren L ^a   Zilli, Eric A ^a  

^a Center for Memory and Brain   (United States)

Author keywords

Episodic memory; Grid cells; Head direction; Hippocampus; Membrane potential oscillations; Place cells; Rat; Theta rhythm

Indexed keywords

EPISODIC MEMORY; GRID CELLS; HEAD DIRECTION; HIPPOCAMPUS; MEMBRANE POTENTIAL OSCILLATIONS; PLACE CELLS; THETA RHYTHM;

ELECTROENCEPHALOGRAPHY; PHASE LOCKED LOOPS;

CELL MEMBRANES;

ARTICLE; BEHAVIOR; ENTORHINAL CORTEX; EPISODIC MEMORY; IMAGINATION; MEMBRANE CURRENT; MEMBRANE POTENTIAL; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; NERVE CELL NETWORK; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RECALL; RECOGNITION; SPIKE WAVE; STIMULUS RESPONSE; WORKING MEMORY;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; ENTORHINAL CORTEX; HUMANS; MEMORY; MODELS, NEUROLOGICAL; NERVE NET; NEURAL INHIBITION; NEURONS; WAKEFULNESS;

EID: 70349382524     PISSN: 08936080     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neunet.2009.07.012     Document Type: Article

References (134)

1. Acker C.D., Kopell N., and White J.A. Synchronization of strongly coupled excitatory neurons: Relating network behavior to biophysics. Journal of Computational Neuroscience 15 1 (2003) 71-90
2. Acquas E., Wilson C., and Fibiger H.C. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: Effects of novelty, habituation, and fear. Journal of Neuroscience 16 9 (1996) 3089-3096
3. Alonso A., and Garcia-Austt E. Neuronal sources of theta rhythm in the entorhinal cortex of the rat. I. Laminar distribution of theta field potentials. Experimental Brain Research 67 3 (1987) 493-501
4. Alonso A., and Klink R. Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. Journal of Neurophysiology 70 1 (1993) 128-143
5. Alonso A., and Llinas R.R. Subthreshold Na-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342 (1989) 175-177
6. Amit D.J., and Brunel N. Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. Cerebral Cortex 7 3 (1997) 237-252
7. Barry C., Fleming S.M., Jeewajee A., O'Keefe J., and Burgess N. Effect of novelty on grid cell firing. Proceedings of the ICCNS 12 (2008) 35
8. Bland B.H. The physiology and pharmacology of hippocampal-formation theta rhythms. Progress in Neurobiology 26 (1986) 1-54
9. Boccara, C.N., Sargolini, F., Hult-Thoresen, V.M., Witter, M.P., Moser, E.I., & Moser, M.-B. (2008). Grid cells in presubiculum and parasubiculum. Paper presented at the Svalbard conference on Hippocampus and Navigation, Svalbard, Norway
10. Brown G.D., Preece T., and Hulme C. Oscillator-based memory for serial order. Psychological Review 107 1 (2000) 127-181
11. Burgess N. Grid cells and theta as oscillatory interference: Theory and predictions. Hippocampus 18 12 (2008) 1157-1174
12. Burgess, N., Barry, C., Jeffery, K.J., & O'Keefe, J. (2005). A grid and place cell model of path integration utilizing phase precession versus theta. Paper presented at the Computational Cognitive Neuroscience Meeting, Computational Cognitive Neuroscience Meeting, Washington, D.C.
13. Burgess N., Barry C., and O'Keefe J. An oscillatory interference model of grid cell firing. Hippocampus 17 9 (2007) 801-812
14. Chow C.C., White J.A., Ritt J., and Kopell N. Frequency control in synchronized networks of inhibitory neurons. Journal of Computational Neuroscience 5 4 (1998) 407-420
15. Clayton N.S., Bussey T.J., and Dickinson A. Can animals recall the past and plan for the future?. Nature Reviews. Neuroscience 4 8 (2003) 685-691
16. Corkin S., Amaral D.G., Gonzalez R.G., Johnson K.A., and Hyman B.T. H. M.'s medial temporal lobe lesion: Findings from magnetic resonance imaging. Journal of Neuroscience 17 10 (1997) 3964-3979
17. Cutsuridis V., Cobb S., and Graham B.P. Encoding and retrieval in a CA1 microcircuit model of the hippocampus. In: Kurkova V., Neruda R., and Koutnik J. (Eds). ICANN 2008, LNCS (2008), Springer-Verlag, Berlin 238-247
18. Cutsuridis V., Cobb S., and Graham B.P. Encoding and retrieval in a model of the hippocampal CA1 microcircuit. Hippocampus (2009)
19. Denham M.J., and Borisyuk R.M. A model of theta rhythm production in the septal-hippocampal system and its modulation by ascending brain stem pathways. Hippocampus 10 6 (2000) 698-716
20. Dhillon A., and Jones R.S. Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro. Neuroscience 99 3 (2000) 413-422
21. Dickson C.T., Magistretti J., Shalinsky M.H., Fransen E., Hasselmo M.E., and Alonso A. Properties and role of I (h) in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. Journal of Neurophysiology 83 5 (2000) 2562-2579
22. Egorov A.V., Hamam B.N., Fransen E., Hasselmo M.E., and Alonso A.A. Graded persistent activity in entorhinal cortex neurons. Nature 420 6912 (2002) 173-178
23. Eichenbaum H., and Cohen N.J. From conditioning to conscious recollection: Memory systems of the brain (2001), Oxford University Press, New York
24. Fransen E., Alonso A.A., Dickson C.T., Magistretti J., and Hasselmo M.E. Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus 14 3 (2004) 368-384
25. Fransén E., Tahvildari B., Egorov A.V., Hasselmo M.E., and Alonso A.A. Mechanism of graded persistent cellular activity of entorhinal cortex layer v neurons. Neuron 49 5 (2006) 735-746
26. Fyhn M., Hafting T., Treves A., Moser M.B., and Moser E.I. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446 7132 (2007) 190-194
27. Gillund G., and Shiffrin R.M. A retrieval model for both recognition and recall. Psych. Rev. 91 1 (1984) 1-67
28. Giocomo L.M., and Hasselmo M.E. Computation by oscillations: Implications of experimental data for theoretical models of grid cells. Hippocampus 18 12 (2008) 1186-1199
29. Giocomo L.M., and Hasselmo M.E. Time constants of h current in layer II stellate cells differ along the dorsal to ventral axis of medial entorhinal cortex. Journal of Neuroscience 28 38 (2008) 9414-9425
30. Giocomo L.M., and Hasselmo M.E. Knock-out of HCN1 subunit flattens dorsal-ventral frequency gradient of medial entorhinal neurons in adult mice. Jounal of Neuroscience 29 (2009) 7625-7630
31. Giocomo L.M., Zilli E.A., Fransen E., and Hasselmo M.E. Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315 5819 (2007) 1719-1722
32. Gorchetchnikov A., and Grossberg S. Space, time and learning in the hippocampus: How fine spatial and temporal scales are expanded into population codes for behavioral control. Neural Networks 20 2 (2007) 182-193
33. Hafting T., Fyhn M., Bonnevie T., Moser M.B., and Moser E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 453 7199 (2008) 1248-1252
34. Hafting T., Fyhn M., Molden S., Moser M.B., and Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 436 (2005) 801-806
35. Hassabis D., Kumaran D., Vann S.D., and Maguire E.A. Patients with hippocampal amnesia cannot imagine new experiences. Proceedings of the National Academy Sciences of the United States of America 104 5 (2007) 1726-1731
36. Hassabis D., and Maguire E.A. Deconstructing episodic memory with construction. Trends in Cognition Science 11 7 (2007) 299-306
37. Hasselmo M.E. Arc length coding by interference of theta frequency oscillations may underlie context-dependent hippocampal unit data and episodic memory function. Learning and Memory 14 11 (2007) 782-794
38. Hasselmo M.E. Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18 12 (2008) 1213-1229
39. Hasselmo M.E. Neuroscience. The scale of experience. Science 321 5885 (2008) 46-47
40. Hasselmo M.E. Temporally structured replay of neural activity in a model of entorhinal cortex, hippocampus and postsubiculum. European Journal of Neuroscience 28 (2008) 1301-1315
41. Hasselmo, M.E. (2009). A model of episodic memory: Mental time travel along encoded trajectories using grid cells and phase coding. Neurobiology of Learning and Memory (in press)
42. Hasselmo M.E., and Brandon M.P. Linking cellular mechanisms to behavior: Entorhinal persistent spiking and membrane potential oscillations may underlie path integration, grid cell firing, and episodic memory. Neural Plast (2008) 658323
43. Hasselmo M.E., and Eichenbaum H. Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Networks 18 9 (2005) 1172-1190
44. Hasselmo M.E., Giocomo L.M., and Zilli E.A. Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17 12 (2007) 1252-1271
45. Hasselmo M.E., Schnell E., and Barkai E. Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. Journal of Neuroscience 15 7 Pt 2 (1995) 5249-5262
46. Hasselmo M.E., and Stern C.E. Mechanisms underlying working memory for novel information. Trends Cogn. Sci. 10 11 (2006) 487-493
47. Heys, J.G., Giocomo, L.M., & Hasselmo, M.E. (2009). Cholinergic modulation of the resonance properties of stellate cells in layer II of medial entorhinal cortex (in review)
48. Hopfield J.J. Neural networks and physical systems with emergent selective computational abilities. Proceedings of the National Academy Sciences of the United States of America 79 (1982) 2554-2559
49. Howard M.W., Fotedar M.S., Datey A.V., and Hasselmo M.E. The temporal context model in spatial navigation and relational learning: Toward a common explanation of medial temporal lobe function across domains. Psychol. Rev. 112 1 (2005) 75-116
50. Howard M.W., and Kahana M.J. A distributed representation of temporal context. Journal of Mathematical Psychology 46 3 (2002) 269-299
51. Jensen O., and Lisman J.E. Hippocampal CA3 region predicts memory sequences: Accounting for the phase precession of place cells. Learning and Memory 3 (1996) 279-287
52. Jensen O., and Lisman J.E. Novel lists of 7 + / - 2 known items can be reliably stored in an oscillatory short-term memory network: Interaction with long-term memory. Learning and Memory 3 (1996) 257-263
53. Jensen O., and Lisman J.E. Theta/gamma networks with slow NMDA channels learn sequences and encode episodic memory: Role of NMDA channels in recall. Learning and Memory 3 (1996) 264-278
54. Jensen O., and Lisman J.E. An oscillatory short-term memory buffer model can account for data on the Sternberg task. Journal of Neuroscience 18 24 (1998) 10688-10699
55. Jensen O., and Lisman J.E. Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends in Neuroscience 28 2 (2005) 67-72
56. Johnson A., and Redish A.D. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. Journal of Neuroscience 27 45 (2007) 12176-12189
57. Kirwan C.B., Bayley P.J., Galvan V.V., and Squire L.R. Detailed recollection of remote autobiographical memory after damage to the medial temporal lobe. Proceedings of the National Academy Sciences of the United States of America 105 7 (2008) 2676-2680
58. Kjelstrup K.B., Solstad T., Brun V.H., Hafting T., Leutgeb S., Witter M.P., et al. Finite scale of spatial representation in the hippocampus. Science 321 5885 (2008) 140-143
59. Kleinfeld D. Sequential state generation by model neural networks. Proceedings of the National Academy Sciences of the United States of America 83 24 (1986) 9469-9473
60. Klink R., and Alonso A. Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. Journal of Neurophysiology 77 4 (1997) 1813-1828
61. Konopacki J., MacIver M.B., Bland B.H., and Roth S.H. Carbachol-induced EEG 'theta' activity in hippocampal brain slices. Brain Research 405 1 (1987) 196-198
62. Kumar S.S., Jin X., Buckmaster P.S., and Huguenard J.R. Recurrent circuits in layer II of medial entorhinal cortex in a model of temporal lobe epilepsy. Journal of Neuroscience 27 6 (2007) 1239-1246
63. Kunec S., Hasselmo M.E., and Kopell N. Encoding and retrieval in the CA3 region of the hippocampus: A model of theta-phase separation. Journal of Neurophysiology 94 1 (2005) 70-82
64. Lengyel M., Szatmary Z., and Erdi P. Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 13 6 (2003) 700-714
65. Leonard B.W., Amaral D.G., Squire L.R., and Zola-Morgan S. Transient memory impairment in monkeys with bilateral lesions of the entorhinal cortex. Journal of Neuroscience 15 8 (1995) 5637-5659
66. Levine B., Svoboda E., Hay J.F., Winocur G., and Moscovitch M. Aging and autobiographical memory: Dissociating episodic from semantic retrieval. Psychology and Aging 17 4 (2002) 677-689
67. Levy W.B. A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus 6 6 (1996) 579-590
68. Lisman J.E. Relating hippocampal circuitry to function: Recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22 2 (1999) 233-242
69. Lisman J.E., Fellous J.M., and Wang X.J. A role for NMDA-receptor channels in working memory. Nature Neuroscience 1 4 (1998) 273-275
70. Lisman J.E., and Idiart M.A. Storage of 7 + / - 2 short-term memories in oscillatory subcycles. Science 267 5203 (1995) 1512-1515
71. Louie K., and Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29 1 (2001) 145-156
72. Matell M.S., and Meck W.H. Cortico-striatal circuits and interval timing: Coincidence detection of oscillatory processes. Brain Research. Cognitive Brain Research 21 2 (2004) 139-170
73. McNaughton B.L., Battaglia F.P., Jensen O., Moser E.I., and Moser M.B. Path integration and the neural basis of the 'cognitive map'. Nature Reviews. Neuroscience 7 8 (2006) 663-678
74. McNaughton B.L., and Morris R.G.M. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends in Neuroscience 10 (1987) 408-415
75. Miall R. The storage of time intervals using oscillating neurons. Neural Computation 1 (1989) 359-371
76. Miller P. Analysis of spike statistics in neuronal systems with continuous attractors or multiple, discrete attractor States. Neural Computation 18 6 (2006) 1268-1317
77. Miller P., and Wang X.J. Power-law neuronal fluctuations in a recurrent network model of parametric working memory. Journal of Neurophysiology 95 2 (2006) 1099-1114
78. Minai A.A., and Levy W.B. Sequence learning in a single trial. Proceedings of the World Congress on Neural Networks 2 (1993) 505-508
79. Mitchell S.J., and Ranck Jr. J.B. Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Research 189 1 (1980) 49-66
80. Moser E.I., and Moser M.B. A metric for space. Hippocampus 18 12 (2008) 1142-1156
81. Netoff T.I., Acker C.D., Bettencourt J.C., and White J.A. Beyond two-cell networks: Experimental measurement of neuronal responses to multiple synaptic inputs. Journal of Computational Neuroscience 18 3 (2005) 287-295
82. Netoff T.I., Banks M.I., Dorval A.D., Acker C.D., Haas J.S., Kopell N., et al. Synchronization in hybrid neuronal networks of the hippocampal formation. Journal of Neurophysiology 93 3 (2005) 1197-1208
83. O'Keefe J., and Burgess N. Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells. Hippocampus 15 7 (2005) 853-866
84. O'Keefe J., Burgess N., Donnett J.G., Jeffery K.J., and Maguire E.A. Place cells, navigational accuracy, and the human hippocampus. Philosophical Transactions of the Royal Society of London B: Biological Sciences 353 1373 (1998) 1333-1340
85. O'Keefe J., and Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3 (1993) 317-330
86. Otto T., and Eichenbaum H. Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. Behavioural Neuroscience 106 5 (1992) 762-775
87. Otto T., Wolf D., and Walsh T.J. Combined lesions of perirhinal and entorhinal cortex impair rats' performance in two versions of the spatially guided radial-arm maze. Neurobiology of Learning and Memory 68 1 (1997) 21-31
88. Pavlides C., and Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. Journal of Neuroscience 8 (1989) 2907-2918
89. Pervouchine D.D., Netoff T.I., Rotstein H.G., White J.A., Cunningham M.O., Whittington M.A., et al. Low-dimensional maps encoding dynamics in entorhinal cortex and hippocampus. Neural Computation 18 11 (2006) 2617-2650
90. Remme M.W.H., Lengyel M., and Gutkin B.S. The role of ongoing dendritic oscillations in single-neuron computation. Society for Neuroscience Abstracts 33 (2007) 251.20
91. Rolls E.T., Stringer S.M., and Elliot T. Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Network 17 4 (2006) 447-465
92. Rotstein H.G., Oppermann T., White J.A., and Kopell N. The dynamic structure underlying subthreshold oscillatory activity and the onset of spikes in a model of medial entorhinal cortex stellate cells. Journal of Computational Neuroscience 21 3 (2006) 271-292
93. Rotstein H.G., Pervouchine D.D., Acker C.D., Gillies M.J., White J.A., Buhl E.H., et al. Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network. Journal of Neurophysiology 94 2 (2005) 1509-1518
94. Samsonovich A., and McNaughton B.L. Path integration and cognitive mapping in a continuous attractor neural network model. Journal of Neuroscience 17 15 (1997) 5900-5920
95. Sargolini F., Fyhn M., Hafting T., McNaughton B.L., Witter M.P., Moser M.B., et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312 5774 (2006) 758-762
96. Schacter D.L., Addis D.R., and Buckner R.L. Remembering the past to imagine the future: The prospective brain. Nature Reviews. Neuroscience 8 9 (2007) 657-661
97. Schon K., Atri A., Hasselmo M.E., Tricarico M.D., LoPresti M.L., and Stern C.E. Scopolamine reduces persistent activity related to long-term encoding in the parahippocampal gyrus during delayed matching in humans. Journal of Neuroscience 25 40 (2005) 9112-9123
98. Schon K., Hasselmo M.E., Lopresti M.L., Tricarico M.D., and Stern C.E. Persistence of parahippocampal representation in the absence of stimulus input enhances long-term encoding: A functional magnetic resonance imaging study of subsequent memory after a delayed match-to-sample task. Journal of Neuroscience 24 49 (2004) 11088-11097
99. Shalinsky M.H., Magistretti J., Ma L., and Alonso A.A. Muscarinic activation of a cation current and associated current noise in entorhinal-cortex layer-II neurons. Journal of Neurophysiology 88 3 (2002) 1197-1211
100. Skaggs W.E., and McNaughton B.L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271 5257 (1996) 1870-1873
101. Solstad T., Moser E.I., and Einevoll G.T. From grid cells to place cells: A mathematical model. Hippocampus 16 12 (2006) 1026-1031
102. Staubli U., Le T.T., and Lynch G. Variants of olfactory memory and their dependencies on the hippocampal formation. Journal of Neuroscience 15 2 (1995) 1162-1171
103. Steffenach H.A., Witter M., Moser M.B., and Moser E.I. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45 2 (2005) 301-313
104. Suddendorf T., and Corballis M.C. Mental time travel and the evolution of the human mind. Genitic, Social, and General Psychology Monographs 123 2 (1997) 133-167
105. Suzuki W.A., Zola-Morgan S., Squire L.R., and Amaral D.G. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. Journal of Neuroscience 13 6 (1993) 2430-2451
106. Tahvildari B., and Alonso A. Morphological and electrophysiological properties of lateral entorhinal cortex layers II and III principal neurons. Journal of Comparative Neurology 491 2 (2005) 123-140
107. Tahvildari B., Fransen E., Alonso A.A., and Hasselmo M.E. Switching between "On" and "Off" states of persistent activity in lateral entorhinal layer III neurons. Hippocampus 17 4 (2007) 257-263
108. Tamamaki N., and Nojyo Y. Preservation of topography in the connections between the subiculum, field CA1, and the entorhinal cortex in rats. Journal of Comparative Neurology 353 3 (1995) 379-390
109. Taube J.S., Muller R.U., and Ranck Jr. J.B. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. Journal of Neuroscience 10 2 (1990) 420-435
110. Taube J.S., Muller R.U., and Ranck Jr. J.B. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. Journal of Neuroscience 10 2 (1990) 436-447
111. Treves A., and Rolls E.T. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2 2 (1992) 189-199
112. Treves A., and Rolls E.T. Computational analysis of the role of the hippocampus in memory. Hippocampus 4 3 (1994) 374-391
113. Tsodyks M.V., Skaggs W.E., Sejnowski T.J., and McNaughton B.L. Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model. Hippocampus 6 3 (1996) 271-280
114. Tulving E. Elements of episodic memory (1983), Oxford University Press, Oxford, UK
115. Tulving E. Episodic memory: From mind to brain. Annual Review of Psychology 53 (2002) 1-25
116. Wallenstein G.V., and Hasselmo M.E. GABAergic modulation of hippocampal population activity: Sequence learning, place field development, and the phase precession effect. Journal of Neurophysiology 78 1 (1997) 393-408
117. Welinder P.E., Burak Y., and Fiete I.R. Grid cells: The position code, neural network models of activity, and the problem of learning. Hippocampus 18 12 (2008) 1283-1300
118. White J.A., Chow C.C., Ritt J., Soto-Trevino C., and Kopell N. Synchronization and oscillatory dynamics in heterogeneous, mutually inhibited neurons. Journal of Computational Neuroscience 5 1 (1998) 5-16
119. Wilson M.A., and McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 265 5172 (1994) 676-679
120. Witter M.P., Griffioen A.W., Jorritsma-Byham B., and Krijnen J.L.M. Entorhinal projections to the hippocampal CA1 region in the rat: An underestimated pathway. Neuroscience Letters 85 2 (1988) 193-198
121. Witter M.P., and Moser E.I. Spatial representation and the architecture of the entorhinal cortex. Trends in Neuroscience 29 12 (2006) 671-678
122. Witter M.P., Naber P.A., van Haeften T., Machielsen W.C., Rombouts S.A., Barkhof F., et al. Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10 4 (2000) 398-410
123. Witter M.P., Wouterlood F.G., Naber P.A., and Van Haeften T. Anatomical organization of the parahippocampal-hippocampal network. Annals of the New York Academy of Sciences 911 (2000) 1-24
124. Yoshida M., and Alonso A. Cell-type specific modulation of intrinsic firing properties and subthreshold membrane oscillations by the m (k v 7)-current in neurons of the entorhinal cortex. Journal of Neurophysiology 98 5 (2007) 2779-2794
125. Yoshida M., Fransen E., and Hasselmo M.E. mGluR-dependent persistent firing in entorhinal cortex layer III neurons. European Journal of Neuroscience 28 (2008) 1116-1126
126. Yoshida M., and Hasselmo M.E. Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. Journal of Neuroscience 29 15 (2009) 4945-4952
127. Young B.J., Otto T., Fox G.D., and Eichenbaum H. Memory representation within the parahippocampal region. Journal of Neuroscience 17 13 (1997) 5183-5195
128. Zilli, E., Yoshida, M., Tahvildari, B., Giocomo, L.M., & Hasselmo, M.E. (2009). Evaluation of the oscillatory interference model of grid cell firing through analysis and measured variability of some biological oscillators (in review)
129. Zilli E.A., and Hasselmo M.E. Analyses of Markov decision process structure regarding the possible strategic use of interacting memory systems. Front Comput. Neurosci. 2 (2008) 6
130. Zilli E.A., and Hasselmo M.E. The influence of Markov decision process structure on the possible strategic use of working memory and episodic memory. PLoS ONE 3 7 (2008) e2756
131. Zilli E.A., and Hasselmo M.E. Modeling the role of working memory and episodic memory in behavioral tasks. Hippocampus 18 2 (2008) 193-209
132. Zipser D., Kehoe B., Littlewort G., and Fuster J. A spiking network model of short-term active memory. Journal of Neuroscience 13 (1993) 3406-3420
133. Zola-Morgan S., Squire L.R., Amaral D.G., and Suzuki W.A. Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. Journal of Neuroscience 9 12 (1989) 4355-4370
134. Zola-Morgan S., Squire L.R., Clower R.P., and Rempel N.L. Damage to the perirhinal cortex exacerbates memory impairment following lesions to the hippocampal formation. Journal of Neuroscience 13 1 (1993) 251-265