Dissociation between dorsal and ventral hippocampal theta oscillations during decision-making

Abstract

Hippocampal theta oscillations are postulated to support mnemonic processes in humans and rodents. Theta oscillations facilitate encoding and spatial navigation, but to date, it has been difficult to dissociate the effects of volitional movement from the cognitive demands of a task. Therefore, we examined whether volitional movement or cognitive demands exerted a greater modulating factor over theta oscillations during decision-making. Given the anatomical, electrophysiological, and functional dissociations along the dorsal-ventral axis, theta oscillations were simultaneously recorded in the dorsal and ventral hippocampus in rats trained to switch between place and motor-response strategies. Stark differences in theta characteristics were found between the dorsal and ventral hippocampus in frequency, power, and coherence. Theta power increased in the dorsal, but decreased in the ventral hippocampus, during the decision-making epoch. Interestingly, the relationship between running speed and theta power was uncoupled during the decision-making epoch, a phenomenon limited to the dorsal hippocampus. Theta frequency increased in both the dorsal and ventral hippocampus during the decision epoch, although this effect was greater in the dorsal hippocampus. Despite these differences, ventral hippocampal theta was responsive to the navigation task; theta frequency, power, and coherence were all affected by cognitive demands. Theta coherence increased within the dorsal hippocampus during the decision-making epoch on all three tasks. However, coherence selectively increased throughout the hippocampus (dorsal to ventral) on the task with new hippocampal learning. Interestingly, most results were consistent across tasks, regardless of hippocampal-dependent learning. These data indicate increased integration and cooperation throughout the hippocampus during information processing.

Figure 1.

Training paradigm. During pretraining rats were first trained on a response task (right turn). Rats were then trained on blocks of place and response trials. Place trials were cued with a flashing light. Next rats were trained on the fixed task with no more than three consecutive trials of the same navigation strategy. After surgery and recovery, the rats were retrained on the fixed task. Rats then commenced the novel place task. Rats were trained to run to a new place goal arm each day during the place trials, while continuing to make a right turn on the response trials. Last, rats commenced the novel response task. Rats were trained to make a left turn (rather than a right turn) during the response trials and go to the original place arm (east arm) during the place trials.

Figure 2.

Trial analysis. a, Each trial was separated into three segments: waiting at the start arm, running to the goal arm (purported decision-making epoch of the maze) and running to the start arm (control epoch). b, Trials were categorized by navigation strategy (place [black arrow] or response [white arrow] trials) and trial difficulty (competitive/cooperative). On a competitive trial place and response strategies indicated different goal locations. On a cooperative trial both place and response strategies indicated the same goal location.

Figure 3.

a, Example placements of dHipp (left) and vHipp (right) electrodes. b, Example trace of dHipp (top) and vHipp (bottom) raw signal. c, Power spectrum density of dHipp (black) and vHipp (gray) electrodes. d, Coherence spectrum between dHipp and vHipp electrodes. Normalized coherence was calculated as more than the 95% of shuffled signals (horizontal line; see Materials and Methods). e, f, Examples of power spectrogram of dHipp (e) and vHipp (f) segmented into the control, waiting, and decision epochs.

Figure 4.

Dissociations in theta frequency. a–c, Peak theta frequency (left) and change in theta frequency during the decision versus the control epoch (right) on the fixed task (a), novel place task (b), and novel response task (c). Peak theta frequency was greater in the dHipp than the vHipp. Peak theta frequency was higher during the decision epoch in both the dHipp and the vHipp, this effect was greater in the dHipp. ⁺p = 0.052, **p < 0.01, ***p < 0.001.

Figure 5.

a, c, e, Average running speed during the control and decision epochs in rats trained on the fixed task (a), novel place task (c), and novel response task (e). Correlation values (r values) between theta power and running speed in the dHipp and the vHipp during the control epoch and decision epoch. Theta power was positively correlated with running speed in both the dHipp and the vHipp on the fixed task (b). d, f, However, the relationship between running speed and theta power was decoupled during the decision-making epoch in the dHipp on the novel place task (d) and novel response task (f). ⁺p = 0.07, *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 6.

Dissociation between dHipp and vHipp theta power during decision-making. dHipp theta power increased during the decision epoch of the maze. In contrast, theta power decreased in the vHipp during the decision epoch. a, d, g, These effects were consistently seen on the fixed task (a), novel place task (d), and novel response task (g). b, e, h, For each day of each rat the theta power ratio (decision epoch theta power/control epoch theta power) was plotted against the running speed ratio (decision epoch running speed/control epoch running speed) for the fixed task (b), novel place task (e), and novel response task (h). The β values for maze segment occupied (location) and running speed are plotted for both the dHipp and the vHipp. Both maze location (decision vs control epoch) and running speed modulated theta power in the dHipp, though maze location consistently had a greater modulating effect. This was also the case in the vHipp, though maze location had the opposite effect. c, f, i, These effects were consistently seen on the fixed task (c), novel place task (f), novel response task (i). ⁺p = 0.06, *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 7.

Coherence along the septotemporal axis during the control and decision epochs. Significant normalized coherence was measured within the dHipp and the vHipp, as well as between the dHipp and the vHipp. a, Fixed task: normalized coherence was greater during the decision epoch within the dHipp (dorsal), no differences were seen within the vHipp (ventral), nor between the dHipp and vHipp (dorsal-ventral). b, Novel place task: normalized theta coherence increased within the dHipp, within the vHipp, as well as between the dHipp and the vHipp during the decision epoch. c, Novel response task: again, normalized theta coherence increased within the dHipp, despite no differences in normalized coherence within the vHipp or between the dHipp and the vHipp. ⁺p = 0.06, *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 8.

Theta power was modulated with learning, both within and across training days. a, e, i, m, q, Percentage correct performance for the first 10 trials and last 10 trials of the fixed task (a), novel place task (e, i), and novel response task (m, q) during acquisition and criterion (see Materials and Methods). Note that daily performance improves during learning acquisitions and asymptotic performance. b, f, j, n, r, Change in running speed during the decision epoch on the fixed task (b), novel place task (f, j), and novel response task (n, r). c, g, k, o, s, Change in dHipp theta power during the decision epoch on the first 10 trials and last 10 trials of the training session on the fixed task (c), novel place task (g, k), and novel response task (o, s). d, h, l, p, t, Change in vHipp theta power during the decision epoch on the first 10 trials than the last 10 trials of the training session on the fixed task (d), novel place task (h, l), and novel response task (p, t). ⁺p = 0.06, *p < 0.05, **p < 0.01, ***p < 0.001.