Increase in hippocampal theta oscillations during spatial decision making

Abstract

The processing of spatial and mnemonic information is believed to depend on hippocampal theta oscillations (5-12 Hz). However, in rats both the power and the frequency of the theta rhythm are modulated by locomotor activity, which is a major confounding factor when estimating its cognitive correlates. Previous studies have suggested that hippocampal theta oscillations support decision-making processes. In this study, we investigated to what extent spatial decision making modulates hippocampal theta oscillations when controlling for variations in locomotion speed. We recorded local field potentials from the CA1 region of rats while animals had to choose one arm to enter for reward (goal) in a four-arm radial maze. We observed prominent theta oscillations during the decision-making period of the task, which occurred in the center of the maze before animals deliberately ran through an arm toward goal location. In speed-controlled analyses, theta power and frequency were higher during the decision period when compared to either an intertrial delay period (also at the maze center), or to the period of running toward goal location. In addition, theta activity was higher during decision periods preceding correct choices than during decision periods preceding incorrect choices. Altogether, our data support a cognitive function for the hippocampal theta rhythm in spatial decision making.

Keywords: LFP; locomotion; oscillations; radial maze; spatial choice; speed.

Fig 1

Experimental design. A: (Top) Schematic representation of the four-arm maze. Dashed lines mark the central area of the maze where rats stay during intertrial intervals; each trial starts after the removal of the central barriers. Circles at the end of each arm denote reward positions; only one position was rewarded per block of 10 trials (METHODS section). (Bottom) Schematic representation of the intertrial interval (DELAY), DM, and RUN periods. B: (Top) Thin gray lines show locomotion trajectories during three representative 10-trial blocks. Thick lines represent the trajectories for DELAY (green), DM (red), and RUN (black) during a single trial. (Bottom) Locomotion speed and distance to reward location for the single trial highlighted in the top panels. Horizontal segments indicate DELAY, DM, and RUN periods colored as above. C: Task performance before (“Training”) and after (“Recording”) surgical implantation of electrodes. D: Locomotion trajectory of a trained rat across four 10-trial blocks within one recording session. Reward location changes from arm to arm at every block in a clockwise manner. Trials from different blocks are represented by different shades of blue. E: Representative cresyl-stained brain section showing glial tracks corresponding to electrodes implanted in the dorsal CA1 region; arrowheads indicate electrode tips. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Fig 2

Behavioral characteristics in the spatial choice task. A: Spatial occupancy for a representative session. B: (Top row) Occupancy in each of the 10-trial blocks in the same session; “R” indicates reward location. (Bottom row) Zoomed in view of spatial occupancy of the central part of the maze during the last 10 s of the intertrial interval. C: Group result of quadrant occupancy ratio, defined as the time spent in the quadrant associated with the rewarded arm divided by the time spent in the other quadrants (see inset for quadrant boundaries). Notice that animals have no preference for the quadrant associated with the rewarded arm during the intertrial interval (P > 0.05, Student's t-test for each occupation ratio against 0.25). D–F: Distribution of DM duration (D), distance traveled (E), and speed (F) during DM across trials. G: Percentage of correct choices on each trial (mean ± SEM over animals). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Fig 3

Theta power increases during DM. A: (First panel) Hippocampal LFP (gray) recorded during a representative trial. Vertical dashed lines mark the moment when barriers were removed and when the animal started to move toward reward location. Horizontal green, red, and black segments indicate intertrial interval (DELAY), DM, and running (RUN) periods, respectively. Notice emergence of robust theta oscillations (5–12 Hz, blue) at the beginning of DM. (Second panel) Wavelet spectrogram showing increased theta energy during DM and RUN. (Third panel) Locomotion speed for the same representative trial. (Fourth panel) Distance from the animal to reward location. B: Group results for percentage energy in the theta band (top), locomotion speed (middle), and distance to reward location (bottom). Solid and dashed lines represent mean ± SEM, respectively (n = 5 animals). Only correct trials were taken into account. C: Mean locomotion speed (left) and normalized theta power (right) during DELAY, DM, and RUN periods. Error bars represent SEM (*P < 0.01, one-way ANOVA followed by Tukey's post hoc test; n = 5 animals). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Fig 4

DM has higher theta power and frequency than delay and running periods in speed-matched conditions. A: Power spectra in speed-matched trials during DELAY (green) and DM (red) for each animal (mean ± SEM over trials). For speed distributions, see Supporting Information Figure S1. B: (Left) Normalized theta power in DM and DELAY (mean ± SEM, n = 5). (Right) Theta peak frequency for the power spectra in A. C,D: The same as above but for DM and RUN periods (*P < 0.05, Student's t-test). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Fig 5

Highest theta power during DM occurs for a wide range of speeds. A,B: Normalized theta power (A) and theta peak frequency (B) as a function of speed during DM (red), RUN (black), and DELAY (green) periods (mean ± SEM over trials across rats). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Fig 6

Correct choices have strongest theta power during DM. A: Speed distribution in subsets of trials used in panels B and C. B: (Left) Mean-normalized power spectra during DM previous to correct (green) and incorrect (red) choices. (Right) Normalized DM theta power (mean ± SEM across rats; *P < 0.05, Student's t-test). C: Theta peak frequency during DM in correct and incorrect trials for each animal. D: Normalized theta power (left) and theta peak frequency (right) as a function of speed during DM that preceded correct (green) or incorrect (red) choices. Data points represent mean ± SEM over trials across rats. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]