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The Journal of Neuroscience, February 27, 2008, 28(9):2274-2286; doi:10.1523/JNEUROSCI.4669-07.2008

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Behavioral/Systems/Cognitive
Gamma Oscillatory Firing Reveals Distinct Populations of Pyramidal Cells in the CA1 Region of the Hippocampus

Timothy J. Senior, John R. Huxter, Kevin Allen, Joseph O'Neill, and Jozsef Csicsvari

Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Oxford OX1 3TH, United Kingdom

Correspondence should be addressed to Jozsef Csicsvari, Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, OX1 3TH Oxford, UK. Email: jozsef.csicsvari{at}pharm.ox.ac.uk

Hippocampal place cells that fire together within the same cycle of theta oscillations represent the sequence of positions (movement trajectory) that a rat traverses on a linear track. Furthermore, it has been suggested that the encoding of these and other types of temporal memory sequences is organized by gamma oscillations nested within theta oscillations. Here, we examined whether gamma-related firing of place cells permits such discrete temporal coding. We found that gamma-modulated CA1 pyramidal cells separated into two classes on the basis of gamma firing phases during waking theta periods. These groups also differed in terms of their spike waveforms, firing rates, and burst firing tendency. During gamma oscillations one group's firing became restricted to theta phases associated with the highest gamma power. Consequently, on the linear track, cells in this group often failed to fire early in theta-phase precession (as the rat entered the place field) if gamma oscillations were present. The second group fired throughout the theta cycle during gamma oscillations, and maintained gamma-modulated firing at different stages of theta-phase precession. Our results suggest that the two different pyramidal cell classes may support different types of population codes within a theta cycle: one in which spike sequences representing movement trajectories occur across subsequent gamma cycles nested within each theta cycle, and another in which firing in synchronized gamma discharges without temporal sequences encode a representation of location. We propose that gamma oscillations during theta-phase precession organize the mnemonic recall of population patterns representing places and movement paths.

Key words: cell assembly; theta oscillation; theta-phase precession; place cells; synchronization; temporal coding

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Received Oct. 15, 2007; revised Jan. 3, 2008; accepted Jan. 4, 2008.

Correspondence should be addressed to Jozsef Csicsvari, Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, OX1 3TH Oxford, UK. Email: jozsef.csicsvari{at}pharm.ox.ac.uk

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