Encoding and retrieval in the CA3 region of the hippocampus: A model of theta-phase separation

Journal of Neurophysiology

Volumn 94, Issue 1, 2005, Pages 70-82

  Kunec, Steve ^a,b   Hasselmo, Michael E ^a   Kopell, Nancy ^a  

^a BOSTON UNIVERSITY   (United States)

^b Boston University Mathematics Department ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN REGION; CALCULATION; CELL TYPE; DENTATE GYRUS; ENTORHINAL CORTEX; HIPPOCAMPUS; INFORMATION; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; MEMORY; NERVE CELL; NERVE CELL NETWORK; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; TASK PERFORMANCE; THETA RHYTHM;

ANIMALS; ENTORHINAL CORTEX; HIPPOCAMPUS; LONG-TERM POTENTIATION; MEMORY; MODELS, NEUROLOGICAL; NERVE NET; NEURAL INHIBITION; NEURAL NETWORKS (COMPUTER); NEURONS; SYNAPSES; THETA RHYTHM; TIME FACTORS;

EID: 21644488218     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00731.2004     Document Type: Article

References (56)

1. Amaral D and Witter M. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31: 571-591, 1989.
2. Barnes C and McNaughton B. Psychobiology of Aging: Problems and Perspectives. New York: Elsevier, 1980, p. 253-272.
3. Barnes C, McNaughton B, Mizumori S, Leonard B, and Lin L. Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog Brain Res 83: 287-300, 1990.
4. Bi GQ and Poo MM. Synaptic modification by correlated activity: Hebb's postulate revisited. Ann Rev Neurosci 24: 139-166, 2001.
5. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, and Buzsaki G. Gamma (40-100 Hz) oscillations in the hippocampus of the behaving rat. J Neurosci 15: 47-60, 1995.
6. Brankack J, Stewart M, and Fox S. Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 310-327, 1993.
7. Brazhnik E and Fox S. Intracellular recordings from the medial septal neurons during hippocampal theta rhythm. Exp Brain Res 114: 442-453, 1997.
8. Brecht M, Singer W, and Engel A. Amplitude and direction of saccadic eye movements depend on the synchronicity of collicular population activity. J Neurophysiol 92: 424-432, 2004.
9. Buzsaki G. Theta oscillations in the hippocampus. Neuron 33: 325-340, 2002.
10. Buzsaki G, Leung L, and Vanderwolf C. Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287: 139-171, 1983.
11. Csicsvari J, Hirase H, Czurko A, Mamiya A, and Buzsaki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19: 274-287, 1999.
12. Csicsvari J, Jamieson B, Wise K, and Buzsaki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37: 311-322, 2003.
13. de Schutter E. Computational Neuroscience: Realistic Modeling for Experimentalists. Boca Raton, FL: CRC Press, 2001.
14. Dickson C, Biella G, and de Curtis M. Evidence for spatial modules mediated by temporal synchronization of carbachol-induced gamma rhythm in medial entorhinal cortex. J Neurosci 20: 7846-7854, 2000a.
15. Dickson C and de Curtis M. Enhancement of temporal and spatial synchronization of entorhinal gamma activity by phase reset. Hippocampus 12: 447-456, 2002.
16. Dickson C, Magistretti J, Shalinsky M, Fransen E, Hasselmo M, and Alonso A. Properties and role of 1 h in the pacing of sub-threshold oscillations in the entorhinal cortex layer II neurons. J Neurophysiol 83: 2562-2579, 2000b.
17. Eichenbaum H and Cohen N. From Conditioning to Conscious Recollection. New York: Oxford Univ. Press, 2003.
18. Ermentrout B. Simulating, Analyzing and Animating Dynamical Systems: A Guide to XPPAUT for Researchers and Students. Philadelphia, PA: SIAM, 2002.
19. Fox S, Wolfson S, and Ranck J Jr. Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Exp Brain Res 62: 495-508, 1986.
20. Fransen E, Alonso A, Dickson C, Magistretti J, and Hasselmo M. Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus 14: 368-384, 2004.
21. NCM in entorhinal neuronal activity during delayed matching tasks. J Neurosci 22: 1081-1097, 2002.
22. Freund T and Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336: 170-173, 1998.
23. Freund T and Buzsaki G. Interneurons of the hippocampus. Hippocampus 6: 347-470, 1996.
24. Gloveli T, Saha S, Dugladze T, Traub R, Whittington M, and Buhl E. Differential involvement of proximal and distal dendrite-targeting interneurons during hippocampal γ oscillations. Proc Physiol Soc 544, 2002.
25. Golding N, Staff N, and Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418: 326-331, 2002.
26. Green J and Arduini A. Hippocampal electrical activity in arousal. J Neurophysiol 17: 533-557, 1954.
27. Hasselmo M, Bodelon C, and Wyble B. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval of prior learning. Neural Comput 14: 793-817, 2002.
28. Hasselmo M and Fehlau B. Differences in the time course of ACh and GABA modulation of excitatory synaptic potentials in the slices of rat hippocampus. J Neurophysiol 86: 1792-1802, 2001.
29. Hasselmo M and Schnell E. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 14: 3898-3914, 1994.
30. Hasselmo M, Schnell E, and Barkai E. Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci 15: 5249-5262, 1995.
31. Hebb D. The Organization of Behavior. New York: Wiley, 1949.
32. Hyman J, Wyble B, Goyal V, Rossi C, and Hasselmo M. Stimulation in the hippocampal region CA1 in behaving rats yields LTP when delivered to the peak of theta and LTD when delivered to the trough. J Neurosci 23: 11725-11731, 2003.
33. Jensen O and Lisman J. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem 3: 279-287, 1996.
34. King C, Recce M, and O'Keefe J. The rhythmicity of cells of the medial septum/diagonal band of Broca in the awake freely moving rat: relationships with behaviour and hippocampal theta. Eur J Neurosci 10: 464-477, 1998.
35. Kitchigina V, Vankov A, Barley C, and Sara S. Novelty-elicited, noradrenaline-dependent enhancement of excitability in the dentate gyrus. Eur J Neurosci 9: 41-47, 1997.
36. Klausberger T, Magill P, Marton L, Roberts J, Cobden P, Buzsaki G, and Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421: 844-848, 2003.
37. Levy W. A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus 6: 579-590, 1996.
38. Lisman J. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interaction. Neuron 22: 233-242, 1999.
39. Lisman J. Long-term potentiation: outstanding questions and attempted synthesis. Phil Trans R Soc Lond B Biol Sci 358: 829-842, 2003.
40. Lisman J and Zhabotinsky A. A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 31: 191-201, 2001.
41. h) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497: 119-130, 1996.
42. McNaughton B. Associative pattern completion in hippocampal circuits: new evidence and new questions. Brain Res Rev 16: 193-220, 1991.
43. O'Keefe J and Recce M. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3: 317-330, 1993.
44. Pavlides C, Greestein Y, Grudman M, and Winson J. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439: 383-387, 1988.
45. Petsche H, Gogolak G, and van Zwieten P. Rhythmicity of septal cell discharges at various levels of reticular excitation. Electroencephalogr Clin Neurophysiol 19: 25-33, 1965.
46. Pinsky P and Rinzel J. Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J Comput Neurosci 1: 39-60, 1994.
47. Rizzuto D, Madsen J, Bromfield E, Schulze-Bonhage A, Seelig D, Aschenbrenner-Scheibe R, and Kahana M. Reset of human neocortical oscillations during a working memory task. Proc Natl Acad Sci USA 100: 7931-7936, 2003.
48. Skaggs W, McNaughton B, Wilson M, and Barnes C. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6: 149-172, 1996.
49. Stewart M and Fox S. Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci 13: 163-169, 1990.
50. Treves A and Rolls E. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2: 189-200, 1992.
51. Treves A and Rolls E. Computational analysis of the role of the hippocampus in memory. Hippocampus 4: 374-391, 1994.
52. Tsodyks M, Skaggs W, Sejnowski T, and McNaughton B. Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6: 271-280, 1996.
53. Wallenstein G and Hasselmo M. GABAergic modulation of hippocampal population activity: sequence learning, place field development and the phase precession effect. J Neurophysiol 393-408, 1997.
54. White J, Klink R, Alonso A, and Kay A. Noise from voltage-gated ion channels may influence neuronal dynamics in the entorhinal cortex. J Neurophysiol 80: 262-269, 1998.
55. Witter M. Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus 3: 33-44, 1993
56. Witter M and Amaral D. Entorhinal cortex of the monkey: V. projections to the dentate gyrus, hippocampus and the subicular complex. J Comp Neurol 307: 437-459, 1991.