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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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.).
The authors declare no competing financial interests.
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Zugaro, M., Monconduit, L. & Buzsáki, G. Spike phase precession persists after transient intrahippocampal perturbation. Nat Neurosci 8, 67–71 (2005) doi:10.1038/nn1369
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