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The Journal of Neuroscience, October 21, 2009, 29(42):13232-13241; doi:10.1523/JNEUROSCI.2270-09.2009

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Behavioral/Systems/Cognitive
Single-Trial Phase Precession in the Hippocampus

Robert Schmidt,^1,2 * Kamran Diba,^3 * Christian Leibold,⁴ Dietmar Schmitz,^2,5,6 György Buzsáki,³ and Richard Kempter^1,2,5,6

¹Institute for Theoretical Biology, Department of Biology, Humboldt-Universität zu Berlin, 10115 Berlin, Germany, ²Bernstein Center for Computational Neuroscience Berlin, 10115 Berlin, Germany, ³Center for Molecular and Behavioral Neurobiology, Rutgers University, Newark, New Jersey 07102, ⁴Department of Biology II, University of Munich, 82152 Planegg-Martinsried, Germany, and ⁵Neuroscience Research Center and ⁶NeuroCure Center for Neurosciences, Charité, Universitätsmedizin Berlin, 10117 Berlin, Germany

Correspondence should be addressed to Robert Schmidt, Institute for Theoretical Biology, Department of Biology, Humboldt-Universität zu Berlin, Invalidenstrasse 43, 10115 Berlin, Germany. Email: r.schmidt{at}biologie.hu-berlin.de

During the crossing of the place field of a pyramidal cell in the rat hippocampus, the firing phase of the cell decreases with respect to the local theta rhythm. This phase precession is usually studied on the basis of data in which many place field traversals are pooled together. Here we study properties of phase precession in single trials. We found that single-trial and pooled-trial phase precession were different with respect to phase-position correlation, phase-time correlation, and phase range. Whereas pooled-trial phase precession may span 360°, the most frequent single-trial phase range was only 180°. In pooled trials, the correlation between phase and position (r = –0.58) was stronger than the correlation between phase and time (r = –0.27), whereas in single trials these correlations (r = –0.61 for both) were not significantly different. Next, we demonstrated that phase precession exhibited a large trial-to-trial variability. Overall, only a small fraction of the trial-to-trial variability in measures of phase precession (e.g., slope or offset) could be explained by other single-trial properties (such as running speed or firing rate), whereas the larger part of the variability remains to be explained. Finally, we found that surrogate single trials, created by randomly drawing spikes from the pooled data, are not equivalent to experimental single trials: pooling over trials therefore changes basic measures of phase precession. These findings indicate that single trials may be better suited for encoding temporally structured events than is suggested by the pooled data.

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Received May 14, 2009; revised Aug. 27, 2009; accepted Aug. 29, 2009.

Correspondence should be addressed to Robert Schmidt, Institute for Theoretical Biology, Department of Biology, Humboldt-Universität zu Berlin, Invalidenstrasse 43, 10115 Berlin, Germany. Email: r.schmidt{at}biologie.hu-berlin.de

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