Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat

Abstract

We examined the activity of single cells of the supramammillary nucleus (SUM), the mammillary body (MB), and adjacent regions of the diencephalon with respect to the hippocampal electroencephalogram (EEG) in urethane-anesthetized rats. Twenty-nine of 170 cells were found to discharge synchronously with the theta rhythm of the hippocampus (theta- related neurons). All of the 29 theta-related cells were localized to the SUM or MB. A subset of theta-related cells of SUM and MB discharged in short-duration bursts comparable to the pyramidal complex spike cells of the hippocampus. In contrast to hippocampal complex spikes, however, which predominantly exhibit this mode of firing during non- theta states, the burst firing of SUM/MB cells was strongly correlated with the theta rhythm. The proportion of bursting neurons was higher in MB than in SUM. Using partial coherence analysis, we examined the relationship between SUM/MB theta-related cells and the two generators of theta of the dorsal hippocampus. The theta-related cells of MB showed a stronger correlation with “CA1” than with “dentate” theta, whereas no such asymmetry was found in the relationship between neuronal firing of SUM cells and the two generators of theta in the hippocampus. The foregoing suggests that the theta-related cells of MB are driven by descending projections from the hippocampal formation (CA1), whereas those of the SUM are not. The SUM and MB are intimately connected with the hippocampal formation--the SUM mainly via ascending projections to the dentate gyrus, and the MB via direct descending projections from the subiculum. Theta-related SUM/MB cells may be directly involved in the generation of theta and/or the transfer of theta rhythmicity to various parts of the limbic system and forebrain.

Decoding signal processing in thalamo-hippocampal circuitry: implications for theories of memory and spatial processing

“…While the anteroventral thalamus does not receive direct inputs from the lateral mammillary nucleus (Shibata, 1992), the populations of directionallytuned neurons in the anteroventral thalamus (Tsanov et al, 2011a;Yoganarasimha et al, 2006) might process descending directional information from the retrosplenial cortex (Wyss and Van Groen, 1992), postsubiculum (van Groen and Wyss, 1990) or from potential direct intra-thalamic projections. This line of research supports the hypothesized interaction of theta and head directional processing within the structures of the Papez's circuit (Kocsis and Vertes, 1994;Vertes et al, 2001). Oscillating networks are considered to provide temporal windows for single cells to suppress or facilitate their synaptic inputs in a coordinated manner (Buzsaki, 2010;Csicsvari et al, 1999).…”

Hippocampal Theta-Phase Modulation of Replay Correlates with Configural-Relational Short-Term Memory Performance: Figure 1.

“…Hippocampal activity could entrain other pacemakers such as cholinergic populations in the basal forebrain (Petsche et al, 1962;Tó th et al, 1993; M. G. or the supramammillary nucleus (Kocsis and Vertes, 1994). Alternatively, the hippocampus (subfield CA1) could synchronize with monosynaptic targets in the entorhinal cortex (Colgin and Moser, 2006) and indirectly use their widespread connectivity.…”

Interaction between neocortical and hippocampal networks via slow oscillations

“…Indeed, these current generators are abolished by atropine (acetylcholine antagonist), but remain intact after lesions of the entorhinal cortex (Buzsáki et al, 1983;Vanderwolf and Leung, 1983;Ylinen et al, 1995b). In addition to the MSDB, the hippocampus receives rhythmic subcortical modulatory inputs from several sources (Kocsis and Vertes, 1994;Vertes and Kocsis, 1997).…”

“…Each class of interneuron has its own preferred phase of discharge (Klausberger et al, 2003;Klausberger et al, 2004). In addition to the hippocampus and entorhinal cortex, thetamodulated neurons have been identified in all limbic structures, including the perirhinal cortex (Muir and Bilkey, 1998), cingulate cortex (Leung and Borst, 1987;Colom et al, 1988), prefrontal cortex (Siapas et al, 2005), amygdala (Pare and Gaudreau, 1996;Collins et al, 1999;Pare and Collins, 2000), anterior thalamus (Vertes et al, 2001), mammillary bodies and the supramammillary nucleus (Kocsis and Vertes, 1994), and the subiculum (Bullock et al, 1990;Anderson and O'Mara, 2003). Some of these networks also generate their own theta fields.…”