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

Abstract

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.

Central relaxin-3 receptor (RXFP3) activation increases ERK phosphorylation in septal cholinergic neurons and impairs spatial working memory

“…Indeed, while there is both old and new evidence for the importance of septal glutamate, GABA and ACh neurons in regulating hippocampal activity and locomotion, navigation and exploration (Fuhrmann et al 2015), septal theta does not always precede hippocampal theta, suggesting that regulation of hippocampal theta activity is better viewed as occurring via a set of functionally interrelated components than via a single entity (Nerad and McNaughton 2006). A better understanding of how septal systems integrate the complex brainstem and telencephalic inputs/functions can be obtained by documenting the cytoarchitectonics and related circuits of the septum.…”

Distribution and targets of the relaxin‐3 innervation of the septal area in the rat

“…This view was strengthened by more recent EEG recordings in freely-moving rats that demonstrated that the integrity of the entire medial and lateral septum-hippocampal network is critical for the generation of theta rhythm (Nerad and McNaughton, 2006). There has also been a consensus over many years that the different types of neurons in the septal area play specific roles in generating theta synchrony, with slow-firing cholinergic neurons facilitating hippocampal firing, and parvalbumin GABAergic neurons that innervate GABAergic hippocampal interneurons driving disinhibition of pyramidal or granule cell inhibition, allowing hippocampal synchrony (Freund and Antal, 1988;Freund and Gulyas, 1997;Toth et al, 1997a;Wu et al, 2000), although more recent studies have questioned the relative importance of different neuron populations in awake animals (e.g.…”

The Hippocamposeptal Pathway Generates Rhythmic Firing of GABAergic Neurons in the Medial Septum and Diagonal Bands: An Investigation Using a Complete Septohippocampal PreparationIn Vitro

“…Because many of these MS/DB GABA neurons are known to project to the hippocampus (Jones et al, 1999;Sotty et al, 2003), they may contribute significantly to the generation and/or modulation of hippocampal theta (Toth et al, 1993). In addition, recent results surprisingly showed that hippocampal theta may be initiated significantly more often in hippocampus than in septum (Nerad and McNaughton, 2006). Therefore, it is possible that local hippocampal theta activity may trigger resonating (I h expressing) MS/DB neurons, which in turn modulates and/or helps generate theta across the hippocampus.…”