Frequency of gamma oscillations routes flow of information in the hippocampus

Gamma oscillations are thought to transiently link distributed cell assemblies that are processing related information(1,2), a function that is probably important for network processes such as perception(1-3), attentional selection(4) and memory(5,6). This 'binding' mechanism requires that spatially distributed cells fire together with millisecond range precision(7,8); 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 similar to 25 to almost 150 Hz(1,9-13). 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 position(14-17), and CA3, a hippocampal subfield essential for storage of such information(14,18,19). 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.