The septal EEG suggests a distributed organization of the pacemaker of hippocampal theta in the rat

Individual neurons in the medial septum and diagonal band fire in phase with, and appear to act as a 'pacemaker' of, the hippocampal theta rhythm. We investigated the relationships of periodic EEG both among various parts of the septum and with dorsal hippocampal theta recorded concurrently in freely moving rats. Most septal sites showed theta rhythm concurrent with hippocampal theta during locomotion. However, periods with theta at hippocampal but not septal sites were more frequent than the reverse. Theta waves in different parts of the septum were synchronized with each other but medial septal sites showed less frequent theta than other sites. The phase delays between medial and lateral septal sites were < 10 ms, suggesting that the hippocampus does not act as a simple relay between the two. Spectral analysis revealed periods (> 5 s) of theta at hippocampal sites co-occurring with rhythms at multiple septal sites that were slower than theta. Even slower were the 'slow septal waves' (mean 2.7 Hz), which were present in the absence of locomotion and did not 'drive' the hippocampus. Our data suggest that the pacemaker of hippocampal theta may best be thought of as a set of functionally differentiated components rather than as a single homogenous unit.