Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing

Hippocampus

Volumn 13, Issue 6, 2003, Pages 700-714

  Lengyel, Máté ^a   Szatmáry, Zoltán ^a   Érdi, Péter ^a,b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b KALAMAZOO COLLEGE   (United States)

Author keywords

Hippocampus; Membrane potential oscillation; Model; Place field; Theta phase precession

Indexed keywords

ANALYTIC METHOD; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITE; DENDRITIC CELL; FREQUENCY ANALYSIS; HIPPOCAMPUS; INFORMATION PROCESSING; MATHEMATICAL COMPUTING; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROBABILITY; PYRAMIDAL NERVE CELL; RAT; REVIEW; SIMULATION; SOMATIC CELL; SPATIAL DISCRIMINATION; TOPOGRAPHY;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; BIOLOGICAL CLOCKS; CELL MEMBRANE; DENDRITES; HIPPOCAMPUS; MODELS, NEUROLOGICAL; NEURAL INHIBITION; ORIENTATION; PYRAMIDAL CELLS; RATS; REACTION TIME; SPACE PERCEPTION; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 0042883679     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.10116     Document Type: Review

References (102)

1. Artemenko DP. 1972. Participation of hippocampal neurons in the generation of theta waves. Neirofiziologiia 4:531-539.
2. Barnes CA, McNaughton BL, Mizumori SJY, Leonard BW, Lin LH. 1990. Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog Brain Res 83:287-300.
3. Bi G, Poo M. 2001. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci 24:139-166.
4. Bland BH, Colom LV. 1993. Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol 41:157-208.
5. Bliss TVP, Lømo T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
6. Booth V, Bose A. 2001. Neural mechanisms for generating rate and temporal codes in model CA3 pyramidal cells. J Neurophysiol 85:2432-2445.
7. Bose A, Recce M. 2001. Phase precession and phase-locking of hippocampal pyramidal cells. Hippocampus 11:204-215.
8. Bose A, Booth V, Recce M. 2000. A temporal mechanism for generating the phase precession of hippocampal place cells. J Comput Neurosci 9:5-30.
9. Brown EN, Frank LM, Tang D, Quirk MC, Wilson MA. 1998. A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J Neurosci 18:7411-7425.
10. Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI. 2002. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296:2243-2246.
11. Bures J, Fenton AA, Kaminsky Y, Zinyuk L. 1997. Place cells and place navigation. Proc Natl Acad Sci U S A 94:343-350.
12. Burgess N, Recce M, O'Keefe J. 1994. A model of hippocampal function. Neural Netw 7:1065-1081.
13. Burwell RD, Amaral DG. 1998. Cortical afferents of the perirhinall postrhinal, and entorhinal cortices of the rat. J Comp Neurol 398:179-205.
14. Buzsáki G. 2000. Theta oscillations in the hippocampus. Neuron 33:325-340.
15. Chapman CA, Lacaille JC. 1990a. Cholinergic induction of theta-frequency oscillations in hippocampal inhibitory interneurons and pacing of pyramidal cell firing. J Neurosci 19:8637-8645.
16. Chapman CA, Lacaille JC. 1999b. Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. J Neurophysiol 81:1296-1307.
17. Csicsvári J, Hirase H, Czurkó A, Mamiya A, Buzsáki G. 1999. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274-287.
18. Derrington AM, Lennie P. 1984. Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J Physiol (Lond) 357:219-240.
19. Eichenbaum H. 1996. Is the rodent hippocampus just for "place"? Curr Opin Neurobiol 6:187-195.
20. Eichenbaum H. 2000. Hippocampus: mapping or memory? Curr Biol 10:R785-R787.
21. Fenton AA, Muller RU. 1998. Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc Natl Sci U S A 95:3182-3187.
22. Firzlaff U, Schuller G. 2001. Cortical representation of acoustic motion in the rufous horseshoe bat, Rhinolophus rouxi. Eur J Neurosci 13:1209-1220.
23. Fischer Y, Gähwiler BH, Thompson SM. 1999. Activation of intrinsic hippocampal theta oscillations by acetylcholine in rat septo-hippocampal cocultures. J Physiol (Lond) 519:405-413.
24. Fox SE, Ranck JB Jr. 1975. Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats. Exp Neurol 49:299-313.
25. Freund TF, Antal M. 1988. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170-173.
26. Freund TF, Buzsáki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347-470.
27. Garcia-Munoz A, Barrio LC, Buno W. 1993. Membrane potential oscillations in CA1 hippocampal pyramidal neurons in vitro: intrinsic rhythms and fluctuations entrained by sinusoidal injected current. Exp Brain Res 97:325-333.
28. Gothard KM, Skaggs WE, Moore KM, McNaughton BL. 1996. Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J Neurosci 16:823-835.
29. Green J, Arduini A. 1954. Hippocampal electrical activity in arousal. J Neurophysiol 17:533-557.
30. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurkó A, Buzsáki G. 2002. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417:738-741.
31. Holscher C. 1999. Synaptic plasticity and learning and memory: LTP and beyond. J Neurosci Res 58:62-75.
32. Huerta PT, Lisman JE. 1995. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillations in CA1 in vitro. Neuron 15:1053-1063.
33. Ingham NJ, Hart HC, McAlpine D. 2001. Spatial receptive fields of inferior colliculus neurons to auditory apparent motion in free field. J Neurophysiol 85:23-33.
34. Jensen O. 2001. Information transfer between rhythmically coupled networks: reading the hippocampal phase code. Neural Comput 13:2743-2761.
35. Jensen O, Lisman JE. 1996. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem 3:279-287.
36. Jensen O, Lisman JE. 2000. Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. J Neurophysiol 83:2602-2609.
37. Jung MW, McNaughton BL. 1993. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:165-182.
38. Kamondi A, Acsády L, Wang XJ, Buzsáki G. 1998. Theta oscillation in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8:244-261.
39. Katona I, Acsády L, Freund TF. 1999. Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus. Neuroscience 88:37-55.
40. Kiss T, Orbán G, Lengyel M, Érdi P. 2001. Intrahippocampal gamma and theta rhythm generation in a network model of inhibitory interneurons. Neurocomputing 38/40:713-719.
41. Knierim JJ, McNaughton BL. 2001. Hippocampal place-cell firing during movement in three-dimensional space. J Neurophysiol 85:105-116.
42. Knierim JJ, McNaughton BL, Poe GR. 2000. Three dimensional spatial selectivity of hippocampal neurons during space flight. Nat Neurosci 3:209-210.
43. Lenck-Santini PP, Save E, Poucet B. 2001. Evidence for a relationship between place-cell spatial firing and spatial memory performance. Hippocampus 11:377-390.
44. Leung LS, Yim CY. 1986. Intracellular records of theta rhythm in hippocampal CA1 cells of the rat. Brain Res 367:323-327.
45. Leung LS, Yim CY. 1991. Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res 553:261-274.
46. Lisman JE. 1997. Burst as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20:38-43.
47. Livingstone MS. 1998. Mechanisms of direction selectivity in macaque V1. Neuron 20:509-526.
48. Lopes da Silva FH, Witter MP, Boeijinga PH, Lohman AH. 1990. Anatomic organization and physiology of the limbic cortex. Physiol Rev 70:453-511.
49. Lorente de Nó R. 1934. Studies on the structure of the cerebral cortex. II. Continuation on the structure of the ammonic system. J Psychol Neurol 46:113-177.
50. Lynch GS, Dunwiddie T, GribkoffV. 1977. Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature 266:737-739.
51. Maaswinkel H, Whishaw IQ 1990. Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation. Behav Brain Res 99:143-152.
52. Magee JC. 2001. Dendritic mechanisms of phase precession in hippocampal CA1 pyramidal neurons. J Neurophysiol 86:528-532.
53. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA. 1995. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15:7079-7094.
54. McNaughton BL, Barnes CA, 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.
55. McNaughton BL, Barnes CA, Meltzer J, Sutherland RJ. 1989. Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp Brain Res 76:485-496.
56. Mehta MR, Barnes CA, McNaughton BL. 1997. Experience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci U S A 94:8918-8921.
57. Mehta MR, Quirk MC, Wilson MA. 2000. Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron 25:707-715.
58. Mizumori SJY, McNaughton BL, Barnes CA, Fox KB. 1989. Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c output: evidence for pattern completion in hippocampus. J Neurosci 9:3915-3928.
59. Mizumori SJY, Barnes CA, McNaughton BL. 1990. Behavioral correlates of theta-on and theta-off cells recorded from hippocampal formation of mature young and aged rats. Exp Brain Res 80:365-373.
60. Muller RU, Kubie JL, Ranck JB Jr. 1987. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7:1935-1950.
61. Muller RU, Bostock E, Taube JS, Kubie JL. 1994. On the directional firing properties of hippocampal place cells. J Neurosci 14:7235-7251.
62. Muller RU, Stead M, Pach J. 1996. The hippocampus as a cognitive graph. J Gen Physiol 107:663-694.
63. Nadel L, Eichenbaum H. 1999. Introduction to the special issue on place cells. Hippocampus 9:341-345.
64. Nelken I, Versnel H. 2000. Responses to linear and logarithmic frequency-modulated sweeps in ferret primary auditory cortex. Eur J Neurosci 12: 549-562.
65. Ngezahayo A, Schachner M, Artola A. 2000. Synaptic activity modulates the induction of bidirectional synaptic changes in adult mouse hippocampus. J Neurosci 20:2451-2458.
66. Nuñez A, Garcia-Austt E, Buno W Jr. 1987. Intracellular theta-rhythm generation in identified hippocampal pyramids. Brain Res 416:289-300.
67. O'Keefe J. 1976. Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78-109.
68. O'Keefe J. 1999. Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus 9:352-364.
69. O'Keefe J, Conway DH 1978. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp Brain Res 31:573-590.
70. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely moving rat. Brain Res 34:171-175.
71. O'Keefe J, Nadel L. 1978. The hippocampus as a cognitive map. Oxford: Clarendon Press.
72. O'Keefe J, Recce ML. 1993. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
73. Orbán G, Kiss T, Lengyel M, Érdi P. 2001. Hippocampal rhythm generation: gamma-related theta-frequency resonance in CA3 interneurons. Biol Cybern 84:123-132.
74. Paulsen O, Sejnowski TJ. 2000. Natural patterns of activity and long-term synaptic plasticity. Curr Opin Neurobiol 10:172-179.
75. Pavlides C, Greenstein YJ, Grudman M, Winson J. 1988. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439:383-387.
76. Petsche H, Stumpf C, Gogolak G. 1962. The significance of the rabbit's septum as a relay station between the mid-brain and the hippocampus. I. The control of hippocampal arousal activity by the septum cells. Electroencephalogr Clin Neurophysiol 14:202-211.
77. Pinsky PF, Rinzel J. 1994. Intrinsic and network rythmogenesis in a reduced Traub model for CA3 neurons. J Comput Neurosci 1:39-60.
78. Poucet B, Save E, Lenck-Santini PP. 2000. Sensory and memory properties of hippocampal place cells. Rev Neurosci 11:95-111.
79. Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr. 1992. The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12:1945-1963.
80. Ramóny Cajal S. 1893. Estructura del asta de Ammon y fascia dentata. An Soc Esp Hist Nat 22:53-114.
81. Rauschecker JP, Harris LR. 1989. Auditory and visual neurons in the cat's superior colliculus selective for the direction of apparent motion stimuli. Brain Res 490:56-63.
82. Redish AD. 1999. Beyond the cognitive map: from place cells to episodic memory. Cambridge, MA: MIT Press.
83. Redish DA, Rosenzweig ES, Bohanick JD, McNaughton BL, Barnes CA. 2000. Dynamics of hippocampal ensemble activity realignment: time versus space. J Neurosci 20:9298-9309.
84. Redish DA, Battaglia FP, Chawla MK, Ekstrom AD, Gerrard JL, Lipa P, Rosenzweig ES, Worley PF, Guzowski JF, McNaughton BL, Barnes CA. 2001. Independence of firing correlates of anatomically proximate hippocampal pyramidal cells. J Neurosci 21:1-6.
85. Rinzel J, Ermentrout B. 1998. Analysis of neural excitability and oscillations. In: Koch C, Segev I, editors. Methods in neuronal modeling. Cambridge, MA: MIT Press. p 251-291.
86. Save E, Nerad L, Poucet B. 2000. Contribution of multiple sensory information to place field stability in hippocampal place cells. Hippocampus 10:64-76.
87. Settanni G, Treves A. 2000. Analytical model for the effects of learning on spike count distributions. Neural Comput 12:1773-1787.
88. Shapiro M. 2001. Plasticity, hippocampal place cells, and cognitive maps. Arch Neurol 58:874-881.
89. Shen J, Barnes CA, McNaughton BL, Skaggs WE, Weaver KL. 1997. The effect of aging on experience-dependent plasticity of hippocampal place cells. J Neurosci 17:6769-6782.
90. Shoykhet M, Doherty D, Simons DJ. 2000. Coding of deflection velocity and amplitude by whisker primary afferent neurons: implications for higher level processing. Somatosens Mot Res 17:171-180.
91. Skaggs WE, McNaughton BL, Gothard KM, Markus EJ. 1993. An information-theoretic approach to deciphering the hippocampal code. In: Hanson SJ, Cowan JD, Giles CL, editors. Advances in neural information processing systems. San Mateo, CA: Morgan Kaufmann. p 1030-1037.
92. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. 1996. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.
93. Tóth K, Freund TF, Miles R. 1997. Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J Physiol (Lond) 500:463-474.
94. Tremblay F, Ageranioti-Belanger SA, Chapman CE. 1996. Cortical mechanisms underlying tactile discrimination in the monkey. I. Role of primary somatosensory cortex in passive texture discrimination. J Neurophysiol 76:3382-3403.
95. Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL. 1996. Population dynamics and theta phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6:271-280.
96. Vanderwolf CH. 1969. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.
97. Wallenstein GV, Hasselmo ME. 1997. GABAergic modulation of hippocampal activity: sequence learning, place field development, and the phase precession effect. J Neurophysiol 78:393-408.
98. Wilson MA, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science 261:1055-1058.
99. Winson J. 1972. Interspecies differences in the occurrence of theta. Behav Biol 7:479-487.
100. Wyble BP, Linster C, Hasselmo ME. 2000. Size of CA1-evoked synaptic potentials is related to theta rhythm phase in rat hippocampus. J Neurophysiol 83:2138-2144.
101. Ylinen A, Soltész I, Bragin A, Penttonen M, Sík A, Buzsáki G. 1995. Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5:78-90.
102. Zhang K, Ginzburg I, McNaughton BL, Sejnowski TJ. 1998. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J Neurophysiol 79:1017-1044.