Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Independent rate and temporal coding in hippocampal pyramidal cells


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.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


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

    CAS  Article  Google Scholar 

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

    CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  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)

    ADS  CAS  Article  Google Scholar 

  7. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford Univ. Press, Oxford, 1978); 〈〉 (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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  Google Scholar 

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

    ADS  CAS  Article  Google Scholar 

Download references


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.

Author information

Authors and Affiliations


Corresponding author

Correspondence to John O'Keefe.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Huxter, J., Burgess, N. & O'Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828–832 (2003).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing