Firing rate and theta-phase coding by hippocampal pyramidal neurons during 'space clamping'

European Journal of Neuroscience

Volumn 11, Issue 12, 1999, Pages 4373-4380

  Hirase, Hajime ^a   Czurkó, András ^a   Csicsvari, Jozsef ^a   Buzsáki, György ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Phase precession; Place cells; Temporal coding; Theta activity

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; HIPPOCAMPUS; INTERNEURON; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; ROTATION; RUNNING; SPACE; THETA RHYTHM; VELOCITY;

ACTION POTENTIALS; ANIMALS; ELECTRODES, IMPLANTED; HIPPOCAMPUS; INTERNEURONS; MALE; MOTOR ACTIVITY; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; ROTATION; SPACE PERCEPTION; THETA RHYTHM;

EID: 0033428887     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1999.00853.x     Document Type: Article

References (58)

1. Adrian, E.D. & Zotterman, Y. (1926) The impulses produced by sensory nerve endings. Part 2. The response of a single end organ. J. Physiol. (Lond.), 61, 151-171.
2. Barlow, H.B. (1972) Single units and sensation: a neuron doctrine for perceptual psychology? Perception, 1, 371-394.
3. Brown, E.N., Frank, L.M., Tang, D., Quirk, M.C. & Wilson, M.A. (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.
4. Buhl, E.H., Halasy, K. & Somogyi, P. (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature, 368, 823-828.
5. Bures, J., Fenton, A.A., Kaminsky, Y. & Zinyuk, L. (1997) Place cells and place navigation. Proc. Natl Acad. Sci. USA, 94, 343-350.
6. Burgess, N. & O'Keefe, J. (1996) Neuronal computations underlying the firing of place cells and their role in navigation. Hippocampus, 6, 749-762.
7. Buzsáki, G. (1989) Two-stage model of memory trace formation: a role for 'noisy' brain states. Neuroscience, 31, 551-570.
8. Buzsáki, G. & Chrobak, J.J. (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr. Opin. Neurobiol., 5, 504-510.
9. Buzsáki, G. & Eidelberg, E. (1982) Direct afferent excitation and long-term potentiation of hippocampal interneurons. J. Neurophysiol., 48, 597-607.
10. Buzsáki, G., Leung, L.W. & Vanderwolf, C.H. (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res., 287, 139-171.
11. Cobb, S.R., Buhl, E.H., Halasy, K., Paulsen, O. & Somogyi, P. (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature, 378, 75-78.
12. Csicsvari, J., Hirase, H., Czurko, A. & Buzsáki, G. (1998) Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron, 21, 179-189.
13. Csicsvari, J., Hirase, H., Czurko, A., Mamiya, A. & Buzsáki, G. (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci., 19, 274-287.
14. Czurko, A., Hirase, H., Csicsvari, J. & Buzsáki, G. (1999) Sustained activation of hippocampal pyramidal cells by 'space clamping' in a running wheel. Eur. J. Neurosci., 11, 344-352.
15. Fox, S.E. (1989) Membrane potential and impedance changes in hippocampal pyramidal cells during theta rhythm. Exp. Brain Res., 77, 283-294.
16. Freund, T.F. & Antal, M. (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature, 336, 170-173.
17. Gallyas, F., Hsu, M. & Buzsáki, G. (1993) Four modified silver methods for thick sections of formaldehyde-fixed mammalian central nervous tissue: 'dark' neurons, perikarya of all neurons, microglial cells and capillaries. J. Neurosci. Meth., 50, 159-164.
18. Georgopoulos, A.P., Kalaska, J.F., Caminiti, R. & Massey, J.T. (1982) On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J. Neurosci., 2, 1527-1537.
19. Gerrard, J.L., Ginzburg, I., Barnes, C.A., Sejnowski, T.J. & McNaughton, B.L. (1995) Accuracy of hippocampal place fields in predicting location is enhanced in the presence of theta rhythm. Soc. Neurosci. Abstr., 21, 942.
20. Gray, C.M. & Singer, W. (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl Acad. Sci. USA, 86, 1698-1702.
21. Hopfield, J.J. (1995) Pattern recognition computation using action potential timing for stimulus representation. Nature, 376, 33-36.
22. Jensen, O. & Lisman, J.E. (1996) Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learning Memory, 3, 279-287.
23. Kamondi, A., Acsady, L., Wang, X.J. & Buzsáki, G. (1998) Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus, 8, 244-261.
24. Kocsis, B., Bragin, A. & Buzsáki, G. (1999) Interdependence of multiple theta generators in the hippocampus: a partial coherence analysis. J. Neurosci., 19, 6200-6212.
25. Konig, P., Engel, A.K. & Singer, W. (1996) Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci., 19, 130-137.
26. Leung, L.W. & Yim, C.Y. (1991) Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res., 553, 261-274.
27. Lisman, J.E. & Idiart, M.A. (1995) Storage of 7 ± 2 short-term memories in oscillatory subcycles. Science, 267, 1512-1515.
28. McNaughton, B.L., Barnes, C.A. & 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.
29. Muller, R.U., Bostock, E., Taube, J.S. & Kubie, J.L. (1994) On the directional firing properties of hippocampal place cells. J. Neurosci., 14, 7235-7251.
30. Muller, R.U., Kubie, J.L. & Ranck, J.B. Jr (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci., 7, 1935-1950.
31. O'Keefe, J. (1991a) An allocentric spatial model for the hippocampal cognitive map. Hippocampus, 1, 230-235.
32. O'Keefe, J. (1991b) The hippocampal cognitive map and navigational strategies. In Paillard, J. (ed.) Brain and Space. Oxford University Press, Oxford, pp. 274-295.
33. O'Keefe, J. & Burgess, N. (1996) Geometric determinants of the place fields of hippocampal neurons [see comments]. Nature, 381, 425-428.
34. 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.
35. O'Keefe, J. & Nadel, L. (1978) Hippocampus as a Cognitive Map. Oxford University Press, Oxford.
36. O'Keefe, J. & Recce, M.L. (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus, 3, 317-330.
37. Quirk, M.C. & Wilson, M.A. (1998) Temporal changes in the firing properties of CA1 pyramidal cells in the freely behaving rat. Soc. Neurosci. Abstr., 24, 1910.
38. Recce, M.L. & O'Keefe, J. (1989) The tetrode: a new technique for multiunit extracellular recording. Soc. Neurosci. Abstr., 15, 1250.
39. Riehle, A., Grun, S., Diesmann, M. & Aertsen, A. (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science, 278, 1950-1953.
40. Rivas, J., Gaztelu, J.M. & Garcia-Austt, E. (1996) Changes in hippocampal cell discharge patterns and theta rhythm spectral properties as a function of walking velocity in the guinea pig. Exp. Brain Res., 108, 113-118.
41. de Ruyter Steveninck, R.R., Lewen, G.D., Strong, S.P., Koberle, R. & Bialek, W. (1997) Reproducibility and variability in neural spike trains. Science, 275, 1805-1808.
42. Shadlen, M.N. & Newsome, W.T. (1994) Noise, neural codes and cortical organization. Curr. Opin. Neurobiol., 4, 569-579.
43. Sik, A., Penttonen, M., Ylinen, A. & Buzsáki, G. (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J. Neurosci., 15, 6651-6665.
44. Skaggs, W.E., McNaughton, B.L., Wilson, M.A. & Barnes, C.A. (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus, 6, 149-172.
45. Thompson, L.T. & Best, P.J. (1989) Place cells and silent cells in the hippocampus of freely-behaving rats. J. Neurosci., 9, 2382-2390.
46. Toth, K., Freund, T.F. & Miles, R. (1997) Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J. Physiol. (Lond.), 500, 463-474.
47. Tsodyks, M.V., Skaggs, W.E., Sejnowski, T.J. & McNaughton, B.L. (1996) Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus, 6, 271-280.
48. Vaadia, E., Bergman, H. & Abeles, M. (1989) Neuronal activities related to higher brain functions-theoretical and experimental implications. IEEE Trans. Biomed. Eng., 36, 25-35.
49. Vinogradova, O.S. (1975) The hippocampus and the orienting reflex. In Sokolov, E.N. & Vinogradova, O.S. (eds), Neuronal Mechanism of the Orienting Reflex. Erlbaum, Hillsdale, NJ, pp. 128-154.
50. Wallenstein, G.V. & Hasselmo, M.E. (1997) GABAergic modulation of hippocampal population activity: sequence learning, place field development, and the phase precession effect. J. Neurophysiol., 78, 393-408.
51. Wiener, S.I. (1996) Spatial, behavioral and sensory correlates of hippocampal CA1 complex spike cell activity: implications for information processing functions. Prog. Neurobiol., 49, 335-361.
52. Wiener, S.I., Paul, C.A. & Eichenbaum, H. (1989) Spatial and behavioral correlates of hippocampal neuronal activity. J. Neurosci., 9, 2737-2763.
53. Wilson, M.A. & McNaughton, B.L. (1993) Dynamics of the hippocampal ensemble code for space. Science, 261, 1055-1058.
54. Wilson, M.A. & McNaughton, B.L. (1994) Reactivation of hippocampal ensemble memories during sleep [see comments]. Science, 265, 676-679.
55. Winson, J. (1976) Hippocampal theta rhythm. II. Depth profiles in the freely moving rabbit. Brain Res., 103, 71-79.
56. Wood, E.R., Dudchenko, P.A. & Eichenbaum, H. (1999) The global record of memory in hippocampal neuronal activity. Nature, 397, 613-616.
57. Ylinen, A., Soltesz, I., Bragin, A., Penttonen, M., Sik, A. & Buzsáki, G. (1995) Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus, 5, 78-90.
58. Zhang, K., Ginzburg, I., McNaughton, B.L. & Sejnowski, T.J. (1998) Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J. Neurophysiol., 79, 1017-1044.