Hippocampal 4-Hz oscillations emerge during stationary running in a wheel and are resistant to medial septum inactivation

Recent studies described 2–4 Hz oscillations in the hippocampus of rats performing stationary locomotion on treadmills and other apparatus. Since the 2–4 Hz rhythm shares common features with theta (5–12 Hz) oscillations—such as a positive amplitude-running speed relationship and modulation of spiking activity—many have questioned whether these rhythms are related or independently generated. Here, we analyzed local field potentials and spiking activity from the dorsal CA1 of rats executing a spatial alternation task and running for ~15 s in a wheel during the intertrial intervals both before and after muscimol injection into the medial septum. We observed remarkable 4-Hz oscillations during wheel runs, which presented amplitude positively correlated with running speed. Surprisingly, the amplitude of 4-Hz and theta oscillations were inversely related. Medial septum inactivation abolished hippocampal theta but preserved 4-Hz oscillations. It also affected the entrainment of pyramidal cells and interneurons by 4-Hz rhythmic activity. In all, these results dissociate the underlying mechanism of 4-Hz and theta oscillations in the rat hippocampus.