Rhythms of the hippocampal network

Abstract

The hippocampal local field potential (LFP) shows three major types of rhythms: theta, sharp wave-ripples and gamma. These rhythms are defined by their frequencies, they have behavioural correlates in several species including rats and humans, and they have been proposed to carry out distinct functions in hippocampal memory processing. However, recent findings have challenged traditional views on these behavioural functions. In this Review, I discuss our current understanding of the origins and the mnemonic functions of hippocampal theta, sharp wave-ripples and gamma rhythms on the basis of findings from rodent studies. In addition, I present an updated synthesis of their roles and interactions within the hippocampal network.

Figure 1. Theta sequences in the hippocampus during spatial memory operations

Successive locations in an animal's trajectory are represented by an ordered series of CA3 or CA1 place cell spikes within individual theta cycles, termed a theta sequence. Shown here is a schematic representation of a path to be taken by a rodent in order to reach a reward (bottom), an ongoing theta rhythm (top), and the theta sequence of place cells for two magnified theta cycles (middle), whereby the place cells are colour coded according to the particular point in the path at which their place field is located. For individual place cells within a theta sequence, spikes occur at progressively earlier theta phases across successive theta cycles, a phenomenon termed theta phase precession. Because of this, spikes at early and late theta phases represent earlier and later locations, respectively, in the trajectory.

Figure 2. Replay during sharp wave-ripples

a| Shown here are spikes from successively activated place cells (top) as a rodent passes through the cells’ place fields in a particular trajectory on a linear track (bottom). Each row of colored tick marks represents spikes from a different place cell (calibration: 500 ms). b| Shown here is an example of a sharp wave-ripple (top), recorded during subsequent rest at the end of the linear track; a bandpass filtered (150-300 Hz) version of the sharp wave-ripple is shown immediately below the raw recording. Spikes from the place cell ensemble are shown to reactivate during the sharp wave-ripple in the same order as in exploration but on a faster time scale. Calibration: 50 ms.

Figure 3. Slow and fast gamma rhythms

Two distinct subtypes of gamma rhythms, termed slow and fast gamma, occur in the hippocampal network. Slow gamma rhythms couple activity in hippocampal subregion CA1 to inputs from CA3. By contrast, fast gamma rhythms in CA1 are entrained by inputs from MEC. Typically, the two subtypes of gamma rhythm do not occur at the same time within CA1. Slow and fast gamma rhythms are also observed in CA3, where fast gamma rhythms are also entrained by inputs from MEC. Examples of slow and fast gamma rhythms recorded from CA1 in a freely behaving rat are shown at the top (calibration: 100 ms) in order to demonstrate their somewhat irregular appearance, while stylized versions of the rhythms are shown below.