Interactions between Hippocampus and Medial Septum during Sharp Waves and Theta Oscillation in the Behaving Rat

Abstract

The medial septal region and the hippocampus are connected reciprocally via GABAergic neurons, but the physiological role of this loop is still not well understood. In an attempt to reveal the physiological effects of the hippocamposeptal GABAergic projection, we cross-correlated hippocampal sharp wave (SPW) ripples or theta activity and extracellular units recorded in the medial septum and diagonal band of Broca (MSDB) in freely moving rats. The majority of single MSDB cells (60%) were significantly suppressed during SPWs. Most cells inhibited during SPW (80%) fired rhythmically and phase-locked to the negative peak of the CA1 pyramidal layer theta waves. Because both SPW and the negative peak of local theta waves correspond to the maximum discharge probability of CA1 pyramidal cells and interneuron classes, the findings indicate that the activity of medial septal neurons can be negatively (during SPW) or positively (during theta waves) correlated with the activity of hippocampal interneurons. We hypothesize that the functional coupling between medial septal neurons and hippocampal interneurons varies in a state-dependent manner.

Interaction between neocortical and hippocampal networks via slow oscillations

“…As is the case with thalamo-cortical spindles in which corticothalamic feedback serves as a synchronizer, hippocampal feedback to the medial septum is crucial for producing widespread synchrony (King et al, 1998). However, the hippocamposeptal feedback path is established by long-range GABAergic interneurons (Sik et al, 1994;Dragoi et al, 1999;Gulyas et al, 2003). The septal and intrahippocampal pathways produce a current source in the CA1 pyramidal layer and a sink in the stratum radiatum of CA1.…”

Mode shifting between storage and recall based on novelty detection in oscillating hippocampal circuits

“…These hippocampo-septal projection cells receive convergent input from large numbers of hippocampal principal cells (Tóth et al, 1993). Hippocampal activity may thus inhibit the septum; indeed, both fimbria stimulation (McLennan and Miller, 1974) and hippocampal sharp waves (Dragoi et al, 1999) were shown to inhibit neuronal activity in the medial septum.…”

“…In this respect it is noteworthy that the few studies addressing the function of the hippocampo-medioseptal pathway were performed in anaesthetized rats, and did not characterize the neurons responding to hippocampal input (McLennan and Miller, 1974;Dragoi et al, 1999). Moreover, the clearest effects of hippocampal influence on septal activity were observed during hippocampal sharp waves, rather than REM-associated theta (Dragoi et al, 1999).…”

Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus

“…These numerous sources of theta generators are believed to be coordinated by the reciprocal connections between the septum and hippocampus (23), but the nature of this spatial-temporal coordination is not well understood (24). Both cholinergic and GABAergic neurons, and a small fraction of VGlut2 immunoreactive neurons (25), are believed to play a critical role in such global coordination (26,27). Although GABAergic neurons of the MS were demonstrated to be entrained at theta frequency, identified cholinergic neurons did not show theta-related discharge pattern (28,29).…”