Behavior-Dependent Coordination of Multiple Theta Dipoles in the Hippocampus

Abstract

Theta (4 -10 Hz) oscillations in the hippocampus are thought to be important for plasticity, temporal coding, learning, and memory. The hippocampal system has been postulated to have two (or more) rhythmic sources of theta oscillations, but little is known about the behavior-dependent interplay of theta oscillations in different subregions and layers of the hippocampus. We tested rats in a hippocampus-dependent delayed spatial alternation task on a modified T-maze while simultaneously recording local field potentials from dendritic and somatic layers of the dentate gyrus, CA3, and CA1 regions using high-density, 96-site silicon probes. We found that while theta oscillations were generally coherent throughout the hippocampus, the power, coherence, and phase of theta oscillations fluctuated in a layer-specific manner, confirming the presence of multiple interdependent dipoles. Layer-dependent changes in the power and coherence of theta oscillations varied with aspects of both the memory and control (non-mnemonic) tasks, but only a small fraction of the variance could be explained by running speed or acceleration. Furthermore, the phase lag between theta oscillations in the CA3 and CA1 pyramidal layers was significantly smaller on the maze arm approaching the T-junction than on other arms of the alternation task or on comparable segments of control tasks. Overall, our findings reveal a consortium of layer-specific theta dipoles (current sinks and sources) generated by the rhythmic flow of ions into and out of hippocampal cells. Moreover, our data suggest that these different theta generators flexibly coordinate hippocampal regions and layers to support behavioral task performance.

Updating hippocampal representations: CA2 joins the circuit

“…It has also been reported that there is a slowing of the frequency of the theta rhythm in CA1 in novel environments [79]. Taken together with the fact that the hippocampus has multiple theta generators, perhaps reflecting input to the individual subfields [72], it will be interesting to see if CA2 contributes to behavior-dependent theta frequency shifts. This may be enabled by novelty-dependent activation of projections from the supramammillary (SuM) nucleus of the hypothalamus, which selectively innervates CA2 and the upper blade of dorsal DG [80,81].…”

“…During active exploration and encoding of novel spatial information, rodent MEC and dorsal hippocampal principal cell and interneuron populations are dominated by theta rhythmic, oscillatory activity at 4-12 Hz (see [71]). Theta rhythms recorded in different subregions are covariant during active behavior [72], but the precise nature and behavioraldependence of underlying cell pair interactions spanning DG, CA3 and CA1 remains to be established. Theta rhythmicity is associated with phase-locking and phase precession of neuronal spiking, and thereby imposes complex timing relationships typically not evident in vitro.…”

Electroencephalographic signals synchronize with behaviors and are sexually dimorphic during the light–dark cycle in reproductive frogs

“…Welch's method with the Hamming window was used to compute power spectra with a resolution of 0.5 Hz. For artifact-free epochs, both absolute eeg total power and spectral power for each band were calculated for each epoch, and transformed into a dB scale (10*log 10 ) (Montgomery et al 2009). To minimize the effects of individual variance on outputs, we performed variance normalization for each subject before statistical analysis, in which the absolute power was divided by its own standard deviation for each electrode placement, each frequency band and each frog (Wang et al 2004).…”

The Multiple Origins and Laminar Topography of the Hippocampal Theta Rhythm

“…Contemporary models of theta generation in the hippocampus posit that rhythmic input from the medial septum and other sources such as intrahippocampal recurrent collaterals and hippocampal voltage-gated ion channels are responsible (Bland and Oddie, 2001;Buzsáki, 2002). In this review, we discuss a recent study (Montgomery et al, 2009) that provides a compelling revision to these models and presents evidence for multiple local theta generators throughout the hippocampus. The authors report that theta oscillations varied between the different layers of the hippocampus and that these differences were, to a large extent, a result of local independent theta dipoles.…”

“…Waveform recordings of LFPs depend on conductivity (or resistivity) of the extracellular medium, local anatomy of neurites and synapses, and the electrode geometry in the extracellular space (Montgomery et al, 2009); interpreting which activity is related to local synaptic events, therefore, requires modeling of these multiple variables. Current-source density (CSD) analysis identifies the location and temporal dynamics of membrane current fluctuations and thus can serve to dissociate some of these variables (Leung, 1990).…”