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Frequency of gamma oscillations routes flow of information in the hippocampus

Abstract

Gamma oscillations are thought to transiently link distributed cell assemblies that are processing related information1,2, a function that is probably important for network processes such as perception1,2,3, attentional selection4 and memory5,6. This ‘binding’ mechanism requires that spatially distributed cells fire together with millisecond range precision7,8; however, it is not clear how such coordinated timing is achieved given that the frequency of gamma oscillations varies substantially across space and time, from 25 to almost 150 Hz1,9,10,11,12,13. Here we show that gamma oscillations in the CA1 area of the hippocampus split into distinct fast and slow frequency components that differentially couple CA1 to inputs from the medial entorhinal cortex, an area that provides information about the animal’s current position14,15,16,17, and CA3, a hippocampal subfield essential for storage of such information14,18,19. Fast gamma oscillations in CA1 were synchronized with fast gamma in medial entorhinal cortex, and slow gamma oscillations in CA1 were coherent with slow gamma in CA3. Significant proportions of cells in medial entorhinal cortex and CA3 were phase-locked to fast and slow CA1 gamma waves, respectively. The two types of gamma occurred at different phases of the CA1 theta rhythm and mostly on different theta cycles. These results point to routeing of information as a possible function of gamma frequency variations in the brain and provide a mechanism for temporal segregation of potentially interfering information from different sources.

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Figure 1: Two bands of gamma oscillations in CA1.
Figure 2: Differential coupling with MEC and CA3 during fast and slow gamma oscillations in CA1.
Figure 3: Interregional synchrony during slow and fast gamma oscillations.
Figure 4: Cell firing patterns during fast and slow gamma oscillations.

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Acknowledgements

We thank A. M. Amundsgaard, K. Haugen, K. Jenssen, E. Sjulstad, R. Skjerpeng and H. Waade for technical assistance, M. P. Witter for assistance with recording site localization, E. J. Henriksen and K. Jezek for donating rats for supplementary analyses, C. A. Barnes for helpful comments on the manuscript and G. Buzsáki and a number of other colleagues for helpful discussions. This work was supported by the Kavli Foundation and a Centre of Excellence grant from the Norwegian Research Council.

Author Contributions L.L.C., O.J., M.-B.M. and E.I.M. planned experiments and analyses, L.L.C., T.D., M.F., T.H. and T.B. collected data, L.L.C., T.D. and O.J. wrote analysis programs, L.L.C. and T.D. analysed data, and L.L.C. and E.I.M. wrote the paper, in collaboration with M.-B.M. All authors discussed the results.

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Correspondence to Laura Lee Colgin or Edvard I. Moser.

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Colgin, L., Denninger, T., Fyhn, M. et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462, 353–357 (2009). https://doi.org/10.1038/nature08573

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