Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Gamma Oscillations in Hippocampus



Nature 462, 353-357 (19 November 2009)

Frequency of gamma oscillations routes flow of information in the hippocampus

Laura Lee Colgin1, Tobias Denninger1,3, Marianne Fyhn1,3, Torkel Hafting1,3, Tora Bonnevie1, Ole Jensen2, May-Britt Moser1 & Edvard I. Moser1


1. Kavli Institute for Systems Neuroscience and Centre for the Biology of Memory, MTFS, Olav Kyrres gate 9, Norwegian University of Science and Technology, NO-7489 Trondheim, Norway

2. Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, P.O. Box 9101, Nijmegen NL-6500 HB, The Netherlands

3. Massachusetts Institute of Technology, The Picower Institute for Learning and Memory; University of California San Francisco, Department of Physiology



Gamma oscillations are thought to transiently link distributed cell assemblies that are processing related information, a function that is probably important for network processes such as perception, attentional selection and memory. This 'binding' mechanism requires that spatially distributed cells fire together with millisecond range precision; 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 Hz.

We investigated the function of gamma frequency variations in the hippocampus, a medial temporal lobe structure that plays a critical role in memory.

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 position, and CA3, a hippocampal subfield essential for storage of such information.

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.

Hippocampal gamma oscillations are thought to arise from two sources, one in the entorhinal cortex (EC) and another intrinsic to the hippocampus.

The estimated current sources during hippocampal gamma oscillations closely match the currents that result from stimulation of the perforant path projection from EC to the hippocampus, indicating that hippocampal gamma may be entrained by direct inputs from EC.

Entorhinal gamma has been reported to be relatively fast (~90 Hz), and high-frequency gamma (~80 Hz) has been reported also in the hippocampus. However, in animals with EC lesions, a slower gamma rhythm (~40 Hz) becomes more apparent in the hippocampus. The pattern of current dipoles for this slower oscillation matches the current profile associated with activation of the Schaffer collateral/commissural pathway from CA3 to CA1.

Collectively, these observations indicate that hippocampal gamma oscillations have multiple origins and raise the possibility that variations in gamma frequency in CA1 reflect alternating synchronization with slow gamma in CA3 and fast gamma in EC.

To test this idea, we sampled neural activity simultaneously from CA1 and either CA3 or layer III of medial entorhinal cortex (MEC) in freely moving rats.

Gamma oscillations in CA1 had two distinct frequency components, a slow gamma range (~2550 Hz) and a fast gamma range (~65140 Hz). For 22 CA1 stratum pyramidale recordings from 16 rats, we quantified the coupling between theta phase and power in the gamma frequency range using cross-frequency analyses, which provide a sensitive measure of the coupling between theta phase and gamma power. We found that theta phase was coupled to power in two separate bands of gamma in nearly all experiments.

The main finding of this study is that CA1 exhibits two distinct frequency bands of gamma oscillations that selectively synchronize CA1 with different sources of afferent input. Slow gamma synchronizes CA1 with CA3, and fast gamma synchronizes CA1 with MEC. Considering that gamma synchronization facilitates interactions between brain regions, the results indicate that fast gamma enhances transmission from MEC to CA1 and that slow gamma promotes signalling from CA3 to CA1.

The results are consistent with previous studies reporting that inputs from EC and CA3 arrive in CA1 at different phases of the theta cycle. Long-term potentiation in CA1 is most easily induced at a particular phase of theta, corresponding to the phase when EC input is maximal. This indicates that the theta phase when EC inputs preferentially arrive may coincide with the time when memory encoding occurs optimally and raises the possibility that the EC-coupled CA1 fast gamma observed in the present study serves to facilitate memory encoding.

Retrieval of information is thought to occur at a different theta phase than memory encoding, during which time CA3 input to CA1 is maximal and incoming signals from EC are suppressed. This idea fits well with the hypothesized memory retrieval function for slow gamma. Separation of afferent inputs to CA1 on different phases of theta is probably important for avoiding re-encoding of previously stored memories and also for reliably distinguishing perceptions of ongoing experiences from internally evoked memories.

The present results raise the possibility that slow and fast gamma play an important role in this separation of inputs by filtering out improperly timed signals from one afferent while facilitating transfer of coherent activity from another. Considering that broadband gamma oscillations occur in other areas, separation of gamma oscillations into discrete frequency channels may be used throughout the brain to enhance interregional communication.

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