Independent rate and temporal coding in hippocampal pyramidal cells

Nature

Volumn 425, Issue 6960, 2003, Pages 828-832

  Huxter, John ^a,c   Burgess, Neil ^a,b   O'Keefe, John ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; ELECTROENCEPHALOGRAPHY; SIGNAL ENCODING;

EPISODIC MEMORIES; TEMPORAL CODING;

BRAIN;

ANIMAL CELL; ARTICLE; CODING; DISSOCIATION; ELECTROENCEPHALOGRAM; HIPPOCAMPUS; MEMORY; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPIKE WAVE; STIMULUS RESPONSE; THETA RHYTHM;

ACTION POTENTIALS; ANIMALS; MALE; MEMORY; MODELS, NEUROLOGICAL; PYRAMIDAL CELLS; RATS; REWARD; RUNNING; SPACE PERCEPTION; THETA RHYTHM;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0242268530     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature02058     Document Type: Article

References (30)

1. O'Keefe, J. & Recce, M. L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330 (1993).
2. O'Keefe, J. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78-109 (1976).
3. O'Keefe, J. in Brain and Space (ed. Paillard, J.) 273-295 (Oxford Univ. Press, Oxford, 1991).
4. Buzsaki, G. Theta oscillations in the hippocampus. Neuron 33, 325-340 (2002).
5. Harris, K. D. et al. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417, 738-741 (2002).
6. Mehta, M. R., Lee, A. K. & Wilson, M. A. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417, 741-746 (2002).
7. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford Univ. Press, Oxford, 1978); 〈www.cognitivemap.net〉 (2003).
8. Burgess, N., Maguire, E. A. & O'Keefe, J. The human hippocampus and spatial and episodic memory. Neuron 35, 625-641 (2002).
9. Squire, L. R. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol Rev. 99, 195-231 (1992).
10. Eichenbaum, H. & Cohen, N. From Conditioning to Conscious Recollection (Oxford Univ. Press, Oxford, 2001).
11. Muller, R. A quarter of a century of place cells. Neuron 17, 813-822 (1996).
12. Skaggs, W. E., McNaughton, B. L., Wilson, M. A. & Barnes, C. A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149-172 (1996).
13. Jensen, O. & Lisman, J. E. Position reconstruction from an ensemble of hippocampal place cells: Contribution of theta phase coding. J. Neurophysiol. 83, 2602-2609 (2000).
14. Yamaguchi, Y., Aota, Y., McNaughton, B. L. & Lipa, P. Bimodality of theta phase precession in hippocampal place cells in freely running rats. J. Neurophysiol. 87, 2629-2642 (2002).
15. McNaughton, B. L., Barnes, C. A. & O'Keefe, J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp. Brain Res. 52, 41-49 (1983).
16. Wiener, S. I., Paul, C. A. & Eichenbaum, H. Spatial and behavioral correlates of hippocampal neuronal activity. J. Neurosci. 9, 2737-2763 (1989).
17. Hirase, H., Czurko, H. H., Csicsvari, J. & Buzsaki, G. Firing rate and theta-phase coding by hippocampal pyramidal neurons during 'space clamping'. Eur. J. Neurosci. 11, 4373-4380 (1999).
18. Ekstrom, A. D., Meltzer, J., McNaughton, B. L. & Barnes, C. A. NMDA receptor antagonism blocks experience-dependent expansion of hippocampal "place fields". Neuron 31, 631-638 (2001).
19. Mehta, M. R., Barnes, C. A. & McNaughton, B. L. Experience-dependent, asymmetric expansion of hippocampal place fields. Proc. Natl Acad. Sci. USA 94, 8918-8921 (1997).
20. Lengyel, M., Szatmary, Z. & Erdi, P. Dynamically detuned oscillators account for the coupled rate and temporal code of place cell firing. Hippocampus 13, 700-714 (2003).
21. Pike, F. G. et al. Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents, J. Physiol. Lond. 529, 205-213 (2000).
22. Kamondi, A., Acsady, L., Wang, X. J. & Buzsaki, G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity-dependent phase-precession of action potentials. Hippocampus 8, 244-261 (1998).
23. Burgess, N., Recce, M. & O'Keefe, J. A model of hippocampal function. Neural Netw. 7, 1065-1081 (1994).
24. Tsodyks, M. V., Skaggs, W. E., Sejnowski, T. J. & McNaughton, B. L. Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model. Hippocampus 6, 271-280 (1996).
25. Jensen, O. & Lisman, J. E. Hippocampal CA3 region predicts memory sequences: Accounting for the phase precession of place cells. Learn. Mem. 3, 279-287 (1996).
26. Wallenstein, G. V. & Hasselmo, M. E. GABAergic modulation of hippocampal population activity: Sequence learning, place field development, and the phase precession effect. J. Neurophysiol. 78, 393-408 (1997).
27. Wood, E. R., Dudchenko, P. A. & Eichenbaum, H. The global record of memory in hippocampal neuronal activity. Nature 397, 613-616 (1999).
28. Moita, M. A., Rosis, S., Zhou, Y., LeDoux, J. E. & Blair, H. T. Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37, 485-497 (2003).
29. Kahana, M. J., Sekuler, R., Caplan, J. B., Kirschen, M. & Madsen, J. R. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399, 781-784 (1999).
30. O'Keefe, J. & Burgess, N. Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425-428 (1996).