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Spike phase precession persists after transient intrahippocampal perturbation

Abstract

Oscillatory spike timing in the hippocampus is regarded as a temporal coding mechanism for space, but the underlying mechanisms are poorly understood. To contrast the predictions of the different models of phase precession, we transiently turned off neuronal discharges for up to 250 ms and reset the phase of theta oscillations by stimulating the commissural pathway in rats. After recovery from silence, phase precession continued. The phase of spikes for the first theta cycle after the perturbation was more advanced than the phase of spikes for the last theta cycle just before the perturbation. These findings indicate that phase advancement that emerges within hippocampal circuitry may be updated at the beginning of each theta cycle by extrahippocampal inputs.

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Figure 1: Single-pulse stimulation of intrahippocampal afferents resets theta and silences spiking activity.
Figure 2: Phase precession is preserved after stimulation-induced perturbation.
Figure 3: Phase precession is preserved after stimulation-induced perturbation.
Figure 4: Assembly coding is maintained after transient perturbation.

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References

  1. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971).

    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. Harris, K.D., Henze, D.A., Hirase, H., Leinekugel, X., Dragoi, G., Czurko, A. & Buzsáki, G. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417, 738–741 (2002).

    Article  CAS  Google Scholar 

  5. 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  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Dragoi, G., Harris, K.D. & Buzsáki, G. Place representation within hippocampal networks is modified by long-term potentiation. Neuron 39, 843–853 (2003).

    Article  CAS  Google Scholar 

  8. 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 

  9. 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 

  10. Lisman, J.E. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22, 233–242 (1999).

    Article  CAS  Google Scholar 

  11. 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 

  12. 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 

  13. Kamondi, A., Acsady, L., Wang, X.J. & Buzsáki, 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 

  14. Bose, A., Booth, V. & Recce, M. A temporal mechanism for generating the phase precession of hippocampal place cells. J. Comput. Neurosci. 9, 5–30 (2000).

    Article  CAS  Google Scholar 

  15. Bose, A. & Recce, M. Phase precession and phase-locking of hippocampal pyramidal cells. Hippocampus 11, 204–215 (2001).

    Article  CAS  Google Scholar 

  16. Booth, V. & Bose, A. Neural mechanisms for generating rate and temporal codes in model CA3 pyramidal cells. J. Neurophysiol. 85, 2432–2445 (2001).

    Article  CAS  Google Scholar 

  17. Yamaguchi, Y. A theory of hippocampal memory based on theta phase precession. Biol. Cybern. 89, 1–9 (2003).

    PubMed  Google Scholar 

  18. Lengyel, M., Szatmary, Z. & Erdi, P. Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 13, 700–714 (2003).

    Article  Google Scholar 

  19. Magee, J.C. A prominent role for intrinsic neuronal properties in temporal coding. Trends Neurosci. 26, 14–16 (2003).

    Article  CAS  Google Scholar 

  20. Koene, R.A., Gorchetchnikov, A., Cannon, R.C. & Hasselmo, M.E. Modeling goal-directed spatial navigation in the rat based on physiological data from the hippocampal formation. Neural Net. 16, 577–584 (2003).

    Article  Google Scholar 

  21. Sato, N. & Yamaguchi, Y. Memory encoding by theta phase precession in the hippocampal network. Neural Comput. 15, 2379–2397 (2003).

    Article  Google Scholar 

  22. Ekstrom, A.D., Meltzer, J., McNaughton, B.L. & Barnes, C.A. NMDA receptor antagonism blocks experience-dependent expansion of hippocampal “place fields”. Neuron 30, 631–638 (2001).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Buzsáki, G. & Czeh, G. Commissural and perforant path interactions in the rat hippocampus. Field potentials and unitary activity. Exp. Brain Res. 43, 429–438 (1981).

    PubMed  Google Scholar 

  25. Buzsáki, G., Grastyan, E., Czopf, J., Kellenyi, L. & Prohaska, O. Changes in neuronal transmission in the rat hippocampus during behavior. Brain Res. 225, 235–247 (1981).

    Article  Google Scholar 

  26. Douglas, R.M., McNaughton, B.L. & Goddard, G.V. Commissural inhibition and facilitation of granule cell discharge in fascia dentata. J. Comp. Neurol. 219, 285–294 (1983).

    Article  CAS  Google Scholar 

  27. Buzsáki, G., Chen, L.S. & Gage, F.H. Spatial organization of physiological activity in the hippocampal region: relevance to memory formation. Prog. Brain Res. 83, 257–268 (1990).

    Article  Google Scholar 

  28. Deadwyler, S.A., West, J.R., Cotman, C.W. & Lynch, G. Physiological studies of the reciprocal connections between the hippocampus and entorhinal cortex. Exp. Neurol. 49, 35–57 (1975).

    Article  CAS  Google Scholar 

  29. Lisman, J.E. & Idiart, M.A. Storage of 7±2 short-term memories in oscillatory subcycles. Science 267, 1512–1515 (1995).

    Article  CAS  Google Scholar 

  30. Gilden, D.L., Thornton, T. & Mallon, M.W. 1/f noise in human cognition. Science 267, 1837–1839 (1995).

    Article  CAS  Google Scholar 

  31. Kudrimoti, H.S., Barnes, C.A. & McNaughton, B.L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 19, 4090–4101 (1999).

    Article  CAS  Google Scholar 

  32. Nadasdy, Z., Hirase, H., Czurkó, A., Csicsvari, J. & Buzsáki, G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19, 9497–9507 (1999).

    Article  CAS  Google Scholar 

  33. Lee, A.K. & Wilson, M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183–1194 (2002).

    Article  CAS  Google Scholar 

  34. Blum, K.I. & Abbott, L.F. A model of spatial map formation in the hippocampus of the rat. Neural Comput. 8, 85–93 (1996).

    Article  CAS  Google Scholar 

  35. 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  CAS  Google Scholar 

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

    Article  Google Scholar 

  37. Csicsvari, J., Hirase, H., Czurko, A. & Buzsáki, 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 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  40. Friedman, H.S. & Priebe, C.E. Estimating stimulus response latency. J. Neurosci. Methods 83, 185–194 (1998).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank M. Hasselmo, J. Lisman, J. Magee, M. Mehta, M. Tsodyks and Y. Yamaguchi for making the prediction of their models explicit after transient inactivation. We also thank K.D. Harris, A. Sirota and D.L. Buhl for assisting with data processing and L. Hazan, E. Pastalkova, S. Montgomery, S. Marguet and S. Royer for commenting on the manuscript. Supported by the National Institutes of Health (G.B.), the Human Frontier Science Program (M.B.Z.) and the French Defense Ministry (L.M.).

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Correspondence to György Buzsáki.

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Zugaro, M., Monconduit, L. & Buzsáki, G. Spike phase precession persists after transient intrahippocampal perturbation. Nat Neurosci 8, 67–71 (2005). https://doi.org/10.1038/nn1369

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