Skip to main content

Thank you for visiting nature.com. 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.

  • Letter
  • Published:

Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells

Abstract

According to the temporal coding hypothesis1, neurons encode information by the exact timing of spikes. An example of temporal coding is the hippocampal phase precession phenomenon, in which the timing of pyramidal cell spikes relative to the theta rhythm shows a unidirectional forward precession during spatial behaviour2,3. Here we show that phase precession occurs in both spatial and non-spatial behaviours. We found that spike phase correlated with instantaneous discharge rate, and precessed unidirectionally at high rates, regardless of behaviour. The spatial phase precession phenomenon is therefore a manifestation of a more fundamental principle governing the timing of pyramidal cell discharge. We suggest that intrinsic properties of pyramidal cells have a key role in determining spike times, and that the interplay between the magnitude of dendritic excitation and rhythmic inhibition of the somatic region is responsible for the phase assignment of spikes4,5.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Relation between theta phase and instantaneous firing rate in pyramidal cells.
Figure 2: Unidirectional nature of the phase shift.
Figure 3: Mean phase as a function of instantaneous rate and its temporal derivative.
Figure 4: Proposed role of adaptation in unidirectional phase precession.

Similar content being viewed by others

References

  1. Singer, W. Synchronization of cortical activity and its putative role in information processing and learning. Annu. Rev. Physiol. 55, 349–374 (1993)

    Article  CAS  Google Scholar 

  2. 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 

  3. 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 

  4. Magee, J. C. Dendritic mechanisms of phase precession in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 86, 528–532 (2001)

    Article  CAS  Google Scholar 

  5. 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 

  6. Adrian, E. D. & Zotterman, Y. The impulses produced by sensory nerve endings. Part 2. The response of a single end organ. J. Physiol. (Lond.) 61, 151–171 (1926)

    Article  CAS  Google Scholar 

  7. Gray, C. M. & Singer, W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl Acad. Sci. USA 86, 1698–1702 (1989)

    Article  ADS  CAS  Google Scholar 

  8. Hopfield, J. J. Pattern recognition computation using action potential timing for stimulus representation. Nature 376, 33–36 (1995)

    Article  ADS  CAS  Google Scholar 

  9. Buzsaki, G. & Chrobak, J. J. Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr. Opin. Neurobiol. 5, 504–510 (1995)

    Article  CAS  Google Scholar 

  10. Vaadia, E. et al. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature 373, 515–518 (1995)

    Article  ADS  CAS  Google Scholar 

  11. Riehle, A., Grun, S., Diesmann, M. & Aertsen, A. Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278, 1950–1953 (1997)

    Article  ADS  CAS  Google Scholar 

  12. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, 1978)

    Google Scholar 

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

    Article  Google Scholar 

  14. Quirk, M. C., Blum, K. I. & Wilson, M. A. Experience-dependent changes in extracellular spike amplitude may reflect regulation of dendritic action potential back-propagation in rat hippocampal pyramidal cells. J. Neurosci. 21, 240–248 (2001)

    Article  CAS  Google Scholar 

  15. Harris, K. D., Hirase, H., Leinekugel, X., Henze, D. A. & Buzsaki, G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32, 141–149 (2001)

    Article  CAS  Google Scholar 

  16. Hirase, H., Czurko, A., 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 

  17. Csicsvari, J., Hirase, H., Mamiya, A. & Buzsaki, G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28, 585–594 (2000)

    Article  CAS  Google Scholar 

  18. Csicsvari, J., Hirase, H., Czurko, A. & Buzsaki, G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 21, 179–189 (1998)

    Article  CAS  Google Scholar 

  19. Harris, K. D., Henze, D. A., Csicsvari, J., Hirase, H. & Buzsaki, G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J. Neurophysiol. 84, 401–414 (2000)

    Article  CAS  Google Scholar 

  20. Csicsvari, J., Hirase, H., Czurko, A., Mamiya, A. & Buzsaki, G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci. 19, 274–287 (1999)

    Article  CAS  Google Scholar 

  21. Henze, D. A. & Buzsaki, G. Action potential threshold of hippocampal pyramidal cells in vivo is increased by recent spiking activity. Neuroscience 105, 121–130 (2001)

    Article  CAS  Google Scholar 

  22. Migliore, M., Cook, E. P., Jaffe, D. B., Turner, D. A. & Johnston, D. Computer simulations of morphologically reconstructed CA3 hippocampal neurons. J. Neurophysiol. 73, 1157–1168 (1995)

    Article  CAS  Google Scholar 

  23. Fisher, N. I. Statistical Analysis of Circular Data (Cambridge Univ. Press, New York, 1993)

    Book  Google Scholar 

Download references

Acknowledgements

This work was supported by the NIH and the Human Frontier Science Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to György Buzsáki.

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

Harris, K., Henze, D., Hirase, H. et al. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417, 738–741 (2002). https://doi.org/10.1038/nature00808

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature00808

This article is cited by

Comments

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.

Search

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