Theta dynamics in rat: speed and acceleration across the Septotemporal axis

Abstract

Theta (6-12 Hz) rhythmicity in the local field potential (LFP) reflects a clocking mechanism that brings physically isolated neurons together in time, allowing for the integration and segregation of distributed cell assemblies. Variation in the theta signal has been linked to locomotor speed, sensorimotor integration as well as cognitive processing. Previously, we have characterized the relationship between locomotor speed and theta power and how that relationship varies across the septotemporal (long) axis of the hippocampus (HPC). The current study investigated the relationship between whole body acceleration, deceleration and theta indices at CA1 and dentate gyrus (DG) sites along the septotemporal axis of the HPC in rats. Results indicate that whole body acceleration and deceleration predicts a significant amount of variability in the theta signal beyond variation in locomotor speed. Furthermore, deceleration was more predictive of variation in theta amplitude as compared to acceleration as rats traversed a linear track. Such findings highlight key variables that systematically predict the variability in the theta signal across the long axis of the HPC. A better understanding of the relative contribution of these quantifiable variables and their variation as a function of experience and environmental conditions should facilitate our understanding of the relationship between theta and sensorimotor/cognitive functions.

Figure 1. Methodological specifications.

A: The rats' position on the 140 cm long maze (y-axis) over time (x-axis). 8 consecutive trials are shown. B (left): Distribution of accelerations for all rats across all recording sessions. Max acceleration = 102.70 cm/s²; max deceleration = −105.74 cm/s² (count units = ×10⁵). B (right): Distribution of speeds for all rats across all recording sessions during acceleration and deceleration (count units = ×10⁴). C: The rats' speed (black) and acceleration (red) as a function of position on the maze for an entire recording session for one rat (∼5 minutes). Acceleration is shown in both running directions in order to emphasize the similar distribution of accelerations/decelerations. D (top): Speed (black) and acceleration (red) as a function of time. 8 consecutive trials are shown in order to visualize the relationship between speed and acceleration/deceleration. D (bottom): A closer look at the first 12 seconds of the top signals, now only the first 3 consecutive trials are shown. E: Relationship between acceleration and theta amplitude (top) and deceleration and theta amplitude (bottom) as a function of “low” and “high” speeds.

Figure 2. Electrode locations, corresponding theta traces & relationship between theta amplitude and speed/acceleration/deceleration.

A: Flatmap representation of the hippocampal formation. Electrode placements are indicated as red dots. Each contour line represents a coronal section. Orange star denotes DG electrode as in B–D (bottom), while black star denotes CA1 electrode as in B–D (top). B (top): Photomicrographs of a representative recording site in septal CA1. Middle photomicrograph shows a close-up (20×) of electrode tip, as denoted by the black arrow. The right photomicrograph depicts the next coronal section for verification that the electrode tract ends. The septal CA1 tract ends in slm. The raw, unfiltered LFP for representative CA1 slm electrode is shown. B (bottom): Same as top (CA1), but for DG. The septal DG tract ends in the gcl. Theta trace for representative DG gcl electrode is shown. C: two-dimensional histogram (density plot) of the relationship between speed and theta amplitude for representative CA1 slm and DG gcl electrodes, as well as speed signal with overlaid theta trace. D: two-dimensional histograms for the relationship between theta amplitude and acceleration/deceleration for the same CA1 slm and DG gcl electrodes (all theta envelope units in 2D histograms = ×10⁻⁴; all count units = ×10³; all p-values<.0001). Abbreviations: sr = stratum radiatum; slm = stratum lacunosum moleculare; mol = molecular layer; gcl = granule cell layer.

Figure 3. Relationship between acceleration, deceleration and theta amplitude.

A: two-dimensional histograms for the relationship between deceleration and theta amplitude, with corresponding filtered theta, speed and acceleration traces for simultaneously recorded CA1 electrodes. All theta envelope units = ×10⁻⁴; all count units = ×10³. B: Electrodes were grouped according to septotemporal position. Mean partial correlation coefficients (controlling for speed) are shown for the relationship between deceleration (blue bar) and theta amplitude as well as for acceleration (red bar) and theta amplitude for CA1. As can be seen, when acceleration is separated into its positive and negative constituents, a differential relationship emerges such that deceleration is more predictive of theta amplitude as compared to acceleration. Theta amplitude was significantly modulated by both acceleration and deceleration across the entirety of the hippocampus for CA1. Additionally, deceleration explained more of the variability in theta amplitude across the entirety of CA1 axis. C: Partial correlation coefficients for the relationship between deceleration and theta amplitude (blue circles) and acceleration and theta amplitude (red circles) as a function of distance from the septal pole for CA1. Each dot represents the partial correlation coefficient between each index (acceleration, deceleration) and theta amplitude plotted as a function of distance from the septal pole. The relationship between deceleration and theta amplitude decreased across the septotemporal axis of CA1. D: Same as A, but for DG. Theta amplitude was significantly modulated by both acceleration and deceleration at septal and midseptotemporal DG sites. Further, deceleration explained more of the variability in theta amplitude than acceleration at DG sites.

Figure 4. Speed, acceleration/deceleration and septal theta amplitude as a function of position on the maze.

A: Three-dimensional scatterplot rotated to a specific view showing the relationship between position on 140-cm maze (x-axis), speed (y-axis), and color-coded for theta amplitude. As can be seen, with increasing and maximal speeds (centered in the middle of the maze) theta amplitude increases. B (left): Same as A, but for acceleration in one direction (rat moving from left to right) as denoted by the black arrows on the x-axis. At high accelerations and high decelerations theta amplitude is low and increases in amplitude at less extreme accelerations. Gray star denotes high accelerations and low theta amplitude, while the black star denotes high decelerations and low theta amplitude. B (right): Two-dimensional histograms depicting the relationship between acceleration and theta amplitude (top) and deceleration and theta amplitude (bottom). C: Filtered theta signal (gray) and theta envelope (black) plotted along with speed (blue) and acceleration (red). As can be seen, there is a sharp reduction of the theta amplitude at extreme accelerations and decelerations, and is more pronounced at high decelerations, as represented by the three-dimensional scatter plot and two-dimensional histograms in B. Gray stars represent time points of maximal acceleration, while black stars represent points of maximal deceleration. D and E: Same as A and B, but for a non-septal electrode. (All theta envelope units = ×10⁻⁴; all count units = ×10³).