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Independent rate and temporal coding in hippocampal pyramidal cells

Abstract

In the brain, hippocampal pyramidal cells use temporal1 as well as rate2 coding to signal spatial aspects of the animal's environment or behaviour. The temporal code takes the form of a phase relationship to the concurrent cycle of the hippocampal electroencephalogram theta rhythm1. These two codes could each represent a different variable3,4. However, this requires the rate and phase to vary independently, in contrast to recent suggestions5,6 that they are tightly coupled, both reflecting the amplitude of the cell's input. Here we show that the time of firing and firing rate are dissociable, and can represent two independent variables: respectively the animal's location within the place field, and its speed of movement through the field. Independent encoding of location together with actions and stimuli occurring there may help to explain the dual roles of the hippocampus in spatial and episodic memory7,8, or may indicate a more general role of the hippocampus in relational/declarative memory9,10.

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Figure 1: Place cell phase of firing correlates best with position.
Figure 2: Phase precession is independent of IFR.
Figure 3: Phase is correlated with track location on low- as well as high-firing-rate runs.
Figure 4: Firing rates differ on fast and slow runs through the field.
Figure 5: Phase precession on the shortened tracks.

References

  1. O'Keefe, J. & Recce, M. L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993)

    Article  CAS  Google Scholar 

  2. O'Keefe, J. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78–109 (1976)

    Article  CAS  Google Scholar 

  3. O'Keefe, J. in Brain and Space (ed. Paillard, J.) 273–295 (Oxford Univ. Press, Oxford, 1991)

    Google Scholar 

  4. Buzsaki, G. Theta oscillations in the hippocampus. Neuron 33, 325–340 (2002)

    Article  CAS  Google Scholar 

  5. Harris, K. D. et al. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417, 738–741 (2002)

    Article  ADS  CAS  Google Scholar 

  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)

    Article  ADS  CAS  Google Scholar 

  7. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford Univ. Press, Oxford, 1978); 〈http://www.cognitivemap.net〉 (2003)

    Google Scholar 

  8. Burgess, N., Maguire, E. A. & O'Keefe, J. The human hippocampus and spatial and episodic memory. Neuron 35, 625–641 (2002)

    Article  CAS  Google Scholar 

  9. Squire, L. R. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195–231 (1992)

    Article  CAS  Google Scholar 

  10. Eichenbaum, H. & Cohen, N. From Conditioning to Conscious Recollection (Oxford Univ. Press, Oxford, 2001)

    Google Scholar 

  11. Muller, R. A quarter of a century of place cells. Neuron 17, 813–822 (1996)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  16. Wiener, S. I., Paul, C. A. & Eichenbaum, H. Spatial and behavioral correlates of hippocampal neuronal activity. J. Neurosci. 9, 2737–2763 (1989)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  ADS  CAS  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  23. Burgess, N., Recce, M. & O'Keefe, J. A model of hippocampal function. Neural Netw. 7, 1065–1081 (1994)

    Article  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  27. Wood, E. R., Dudchenko, P. A. & Eichenbaum, H. The global record of memory in hippocampal neuronal activity. Nature 397, 613–616 (1999)

    Article  ADS  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  ADS  CAS  Google Scholar 

  30. O'Keefe, J. & Burgess, N. Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425–428 (1996)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank C. Lever, F. Cacucci, T. Wills, J. Ryan, D. Edwards and T. Hartley for technical assistance. This work was supported by the MRC and the Wellcome Trust. J.H. was a Rothermere Fellow.

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Correspondence to John O'Keefe.

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Huxter, J., Burgess, N. & O'Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828–832 (2003). https://doi.org/10.1038/nature02058

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