Theta variation and spatiotemporal scaling along the septotemporal axis of the hippocampus

Abstract

Hippocampal theta has been related to locomotor speed, attention, anxiety, sensorimotor integration and memory among other emergent phenomena. One difficulty in understanding the function of theta is that the hippocampus (HPC) modulates voluntary behavior at the same time that it processes sensory input. Both functions are correlated with characteristic changes in theta indices. The current review highlights a series of studies examining theta local field potential (LFP) signals across the septotemporal or longitudinal axis of the HPC. While the theta signal is coherent throughout the entirety of the HPC, the amplitude, but not the frequency, of theta varies significantly across its three-dimensional expanse. We suggest that the theta signal offers a rich vein of information about how distributed neuronal ensembles support emergent function. Further, we speculate that emergent function across the long axis varies with respect to spatiotemporal scale. Thus, septal HPC processes details of the proximal spatiotemporal environment while more temporal aspects process larger spaces and wider time-scales. The degree to which emergent functions are supported by the synchronization of theta across the septotemporal axis is an open question. Our working model is that theta synchrony serves to bind ensembles representing varying resolutions of spatiotemporal information at interdependent septotemporal areas of the HPC. Such synchrony and cooperative interactions along the septotemporal axis likely support memory formation and subsequent consolidation and retrieval.

Keywords: dorsoventral axis; entorhinal cortex; hippocampus; locomotor activity; sensorimotor integration; septotemporal axis; theta oscillations.

Figure 1

The topography of EC to HPC projections. (A) Distinct areas of the provide afferents to the septal 50% of the EC (red), the midseptotemporal 25% (blue) and the temporal 25% (yellow) for DG (left) and CA1 (right). EC projections from layer 2 to the DG and CA3 as well as layer 3 to CA1 exhibit a similar topography. Bands or zones of neurons across the entire rostrocaudal extent of the EC innervate progressively more temporal DG, CA3 and CA1 neurons starting from the caudolateral extreme of the EC toward the more medial aspects of the EC. (B, left) cholera toxin b (CTB) injection in septal DG labels rostrocaudal extent of the lateral band (subjacent rhinal sulcus) of EC. Sequential coronal EC sections illustrate labeled (black) EC layer 2 neurons. (B, bottom left) Note labeling along rhinal sulcus (left side of map) and caudal extremes (bottom edge). Black dotted line indicates division of traditional medial (bottom right) and lateral (top left) EC. (B, right) CTB injection in septal CA1 labels neurons in EC layer 3 with a similar topographic distribution within the lateral band of the EC.

Figure 2

Theta LFP signal varies across regions and its relationship to locomotor speed within septal HPC. While fairly coherent within the same septotemporal area, the theta signal varies across lamina within a region (e.g., CA1 stratum radiatum vs. stratum oriens; not shown) and across regions (concurrent CA1 (A) vs. DG (B) recordings illustrated). The relationship of theta to speed is typically strongest with rats running on a linear track in a highly stereotyped manner and diminishes with multiple aspects of sensorimotor experience (e.g., turns, sensory events, task and memory demands; see text for details). (A) Illustration evidences theta variation in relation to speed at concurrently recorded CA1 and (B) DG sites for a single 20 s sweep. Theta amplitude to speed traces (left) illustrate relationship over concurrent 5 min recording session while rat navigated on a linear track (see Hinman et al., ; Long et al., 2014a). As illustrated, CA1 electrodes typically exhibit a much stronger relation to speed than concurrently recorded DG sites.

Figure 3

Theta amplitude varies across the septotemporal axis and the relationship to locomotor speed systematically diminishes with distance from the septal pole of the HPC. (A) Septal most CA1 sites exhibit the strongest relationship to variation in locomotor speed. (B) Sites at the more temporal extremes often exhibit no significant variation in relationship to speed. Notably the relationship of theta to speed is best observed in rats traversing linear tracks (back and forth) and this relationship typically diminishes with turns, task demands, as well as the presentation of sensory events. Illustration indicates example where variation in relation to speed is evident at more septal CA1 stratum lacunosum-moleculare (slm) site as compared to concurrently recorded midseptotemporal site roughly 5mm from septal pole for a single 20 s sweep. Theta amplitude to speed traces (left) illustrate relationship over concurrent 5 min recording session while rat navigated on a linear track (see Hinman et al., ; Long et al., 2014a).

Figure 4

Theta LFP increases irrespective of locomotor speed during exposure to a novel spatial environment. (Figures adapted from Penley et al. (2013), Frontiers in Neuroscience). (A) Baseline theta power values in CA1 and the DG as a function of the average trial speed for a single animal in the familiar condition (black), on the modified path (red), and in the novel space (blue). (B) Distribution of β-values (standardized regression coefficient) from individual electrode sites within the DG (left) and CA1 (right) at different septotemporal positions. Points indicate changes in the power of theta power on the modified path (red) and novel space (blue) from the familiar condition. (C) β-values for coherence across all electrode pairs within septal, across septal, and mid-septotemporal sites and across septal and temporal sites comparing changes in the modified path (red) and novel space (blue) from the familiar condition for DG pairs (right column) and CA1 pairs (left column). For categorical variables (familiar vs. novel space), β-values indicate changes in theta power and coherence independent of alterations in locomotor speed (see Hinman et al., ; Penley et al., ; see also Long et al., / for additional information with regards to β-values for continuous variables).

Figure 5

Novel sound presentation decreases the relationship between theta amplitude and locomotor speed in a location specific manner. Rats were trained to run on a rectangular maze for a food reward. (A) and (B) illustrate a significant decrease in the relationship between speed and theta for septal (A) and temporal (B) electrodes on Arm 2, which was the arm that was in closest proximity to the sound source (see Long et al., for additional details). Surprisingly, we observed a unique reduction in the speed to theta relationship only on the arm nearest the sound source with a habituation of this decreased slope across repeated sound exposures (right).