Erik W. Schomburg

When monitoring neural activity using intracranial electrical recordings, researchers typically consider the signals to have two primary components: fast action potentials (APs) from neurons near the electrode, and the slower local field potential (LFP), thought to be dominated by postsynaptic currents integrated over a larger volume of tissue. In general, a decrease in signal power with increasing frequency is observed for most brain rhythms. The 100-200 Hz oscillations in the rat hippocampus, including "fast gamma" or "epsilon" oscillations and sharp wave-ripples (SPW-Rs), are one exception, showing an increase in power with frequency within this band. We have used detailed biophysical modeling to investigate the composition of extracellular potentials during fast oscillations in rat CA1. We find that postsynaptic currents exhibit a decreasing ability to generate large-amplitude oscillatory signals at high frequencies, whereas phase-modulated spiking shows the opposite trend. Our estimates indicate that APs and postsynaptic currents contribute similar proportions of the power contained in 140-200 Hz ripples, and the two combined generate a signal that closely resembles in vivo SPW-Rs. Much of the AP-generated signal originates from neurons further than 100 μm from the recording site, consistent with ripples appearing similarly strong regardless of whether or not they contain recognizable APs. Additionally, substantial power can be generated in the 90-150 Hz epsilon band by the APs of rhythmically firing pyramidal neurons. Thus, high-frequency LFPs may generally contain signatures of local cell assembly activation.

A topographical relationship exists between the septotemporal segments of the hippocampus and their entorhinal-neocortical targets, but the physiological organization of activity along the septotemporal axis is poorly understood. We recorded sharp-wave ripple patterns in rats during sleep from the entire septotemporal axis of the CA1 pyramidal layer. Qualitatively similar ripples emerged at all levels. From the local seed, ripples traveled septally or temporally at a speed of ∼0.35 m/s, and the spatial spread depended on ripple magnitude. Ripples propagated smoothly across the septal and intermediate segments of the hippocampus, but ripples in the temporal segment often remained isolated. These findings show that ripples can combine information from the septal and intermediate hippocampus and transfer integrated signals downstream. In contrast, ripples that emerged in the temporal pole broadcast largely independent information to their cortical and subcortical targets.