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BIOLOGICAL SCIENCES / NEUROSCIENCE
Hippocampal place cell assemblies are speed-controlled oscillators

Caroline Geisler, David Robbe, Michaël Zugaro^*, Anton Sirota, and György Buzsáki

Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, 197 University Avenue, Newark, NJ 07102

Edited by Nancy J. Kopell, Boston University, Boston, MA, and approved March 28, 2007 (received for review November 14, 2006)

The phase of spikes of hippocampal pyramidal cells relative to the local field oscillation shifts forward ("phase precession") over a full cycle as the animal crosses the cell's receptive field ("place field"). The linear relationship between the phase of the spikes and the travel distance within the place field is independent of the animal's running speed. This invariance of the phase–distance relationship is likely to be important for coordinated activity of hippocampal cells and space coding, yet the mechanism responsible for it is not known. Here we show that at faster running speeds place cells are active for fewer cycles but oscillate at a higher frequency and emit more spikes per cycle. As a result, the phase shift of spikes from cycle to cycle (i.e., temporal precession slope) is faster, yet spatial-phase precession stays unchanged. Interneurons can also show transient-phase precession and contribute to the formation of coherently precessing assemblies. We hypothesize that the speed-correlated acceleration of place cell assembly oscillation is responsible for the phase–distance invariance of hippocampal place cells.

cell assembly | interneurons | phase locking | phase precession | oscillations

*Present address: CNRS-Collège de France, LPPA, 11 Place Marcelin Berthelot, 75005 Paris, France.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/cgi/content/full/0610121104/DC1.

To whom correspondence should be addressed. E-mail: buzsaki{at}rutgers.edu

© 2007 by The National Academy of Sciences of the USA

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