Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task

Abstract

The striatum and hippocampus are conventionally viewed as complementary learning and memory systems, with the hippocampus specialized for fact-based episodic memory and the striatum for procedural learning and memory. Here we directly tested whether these two systems exhibit independent or coordinated activity patterns during procedural learning. We trained rats on a conditional T-maze task requiring navigational and cue-based associative learning. We recorded local field potential (LFP) activity with tetrodes chronically implanted in the caudoputamen and the CA1 field of the dorsal hippocampus during 6-25 days of training. We show that simultaneously recorded striatal and hippocampal theta rhythms are modulated differently as the rats learned to perform the T-maze task but nevertheless become highly coherent during the choice period of the maze runs in rats that successfully learned the task. Moreover, in the rats that acquired the task, the phase of the striatal-hippocampal theta coherence was modified toward a consistent antiphase relationship, and these changes occurred in proportion to the levels of learning achieved. We suggest that rhythmic oscillations, including theta-band activity, could influence not only neural processing in cortico-basal ganglia circuits but also dynamic interactions between basal ganglia-based and hippocampus-based forebrain circuits during the acquisition and performance of learned behaviors. Experience-dependent changes in coordination of oscillatory activity across brain structures thus may parallel the well known plasticity of spike activity that occurs as a function of experience.

Fig. 1.

Simultaneously recorded LFP oscillations in the caudoputamen and the CA1 field of the dorsal hippocampus exhibit distinguishable task-related modulation during instructed running in a T-maze task. (A) Nissl-stained transverse sections illustrating, at arrows, the tracks of tetrodes in the medial caudoputamen (Left) and the CA1 pyramidal cell layer (Right). CP, caudoputamen; CA1, hippocampal CA1 field; DG, dentate gyrus. (Scale bars: 1 mm.) (B) T-maze with task events. (C) Raw striatal LFP trace recorded during a single representative trial. (D and E) Mean power (red) with 95% confidence limits (black) of LFP activity in the striatum (Left) and hippocampus (Right) during a 0.75-s epoch after tone onset and plotted on linear (D) and log (E) scales. Data were averaged across values for three rats (S23, acquisition session 7; S31, acquisition session 5, S36, acquisition session 10) during the session in which each reached running-time asymptote. (F) Reconstructed spectrograms of LFP activity in the medial striatum (Upper) and in the dorsal hippocampus (Lower) averaged for data from the three rats at their running-time asymptotes, as in D. The task time was reconstructed by abutting individual peri-event windows (bracketed by white vertical lines) with widths reflecting median inter-event intervals. Labeled task event times are indicated by black vertical lines. Data are plotted as normalized power relative to pretrial baseline activity on pseudocolor log scales at the right.

Fig. 2.

LFP oscillations in the striatum and the hippocampus exhibit different task-dependent modulation. (A) Average spectral power in four frequency bands of LFPs recorded in the medial striatum (Left) and the hippocampus (Right) averaged across values for the three rats (S17, S31, and S36). Black lines indicate upper and lower 95% confidence limits. Alternating white and shaded zones indicate time windows around task events. W, warning click; Ga, gate opening; To, instruction tone onset; TS, turn start; TE, turn end; G, goal reaching. (B and C) Correlations of broad-band theta power (5–12 Hz) in the medial striatum (dark blue) and hippocampus (green) with movement velocity (B) and acceleration (C) of three individual rats [(Left) S17, acquisition session 8. (Center) S18, acquisition session 6. (Right) S23, acquisition session 7] sampled at 101-ms intervals during the 2.5 s before and 0.5 s after goal reaching in each trial. Each dot represents one such sample. Power is normalized to the median of all points within each recording site and session.

Fig. 3.

The coherence between striatal and hippocampal theta-band LFP oscillations is the strongest at the decision period of the maze runs. (A) Single-session average coherogram (S17, acquisition session 8), assembled by abutting six peri-event striatal–hippocampal coherograms, smoothed with two tapers (width = 3). Window widths reflect median inter-event intervals. The average coherence values are indicated in pseudocolor according to the scale at the right. (B) Plots of session-averaged coherence magnitude (black lines) and phase (green arrows) showing the dynamics of the synchrony between the striatal and hippocampal signals. The phase angle of significantly coherent signals is indicated by the direction of green arrows (up, 0°; down, 180°; left, 90° lead or 270° lag of hippocampus relative to striatum). Horizontal red lines indicate the level of significant coherence. Black arrows mark 9 Hz.

Fig. 4.

Coherence of striatal and hippocampal theta-band LFP oscillations increases in rats that successfully learn the T-maze task. (A and B) Performance accuracy (A) and running times (B) of each rat during training on the procedural T-maze task. Four rats (S17, light blue; S18, purple; S23, dark blue; S36, green) reached the acquisition criterion, but two rats (S31, red; S35, orange) did not. (C) Average magnitude of peak coherence in a 7- to 11-Hz band during 0.75-s pretrial baseline (BL), post-tone, and pre-goal periods. Each line represents coherence values for a single rat that learned the task, and averaged over all sessions for each rat (color-coded as in A). Error bars indicate standard errors of the mean. (D) Average magnitude of coherence in theta-band oscillations during 0.75-s pre-trial baseline, tone, and goal periods for the four learners (blue) and the two nonlearners (red). (E and F) Changes in coherence during the post-tone period relative to pre-trial baseline. Data from individual rats are color-coded as in A. Significant increases in coherence magnitude of striatal–hippocampal theta were found for all learners but not for non-learners in averages across all sessions (ANOVA, F = 54.42, P < 0.0001) (E) and also in averages across the first five available training sessions (ANOVA, F = 45.21, P < 0.0001) (F), during which behavioral performance of the learners and non-learners was comparable (SI Fig. 10 A and B). (G–I) Values for coherence magnitude at 9 Hz (G), running velocity (H), and acceleration (I) calculated for pre- and postevent periods for six task events (as described for Fig. 2A) averaged over all sessions for each rat (color-coded as in A).

Fig. 5.

The phase of striatal–hippocampal theta coherence is modulated during learning. (A) Average phase angles plotted for the six rats whose percent correct and running times are shown in the same color codes as in Fig. 3. Coherence phase was calculated by subtracting the striatal phase from the hippocampal phase and converting the angles to a 0–360° range. (B) Phase angles during the posttone period for the first to last training sessions for individual rats are shown from center to periphery of the polar plots. (C) Coherence phase angles measured at three task periods during individual sessions up to asymptote of running speed for rats S17 (1 session), S18 (2 sessions), S23 (3 sessions), and S36 (1 session). (D–I) Amounts of change in coherence phase angles from pretrial baseline period to posttone period (D–F) and from posttone period to pregoal period (G–I) during T-maze training for the four learners. Changes in coherence phase angles from pretrial baseline to posttone period were significantly correlated with learning stage (R = 0.46, P < 0.05) (D) and with running time (R = −0.48, P < 0.02) (F) but not with percent-correct response (R = 0.35, P = 0.079) (E). Tone-to-goal changes in coherence phase angles were significantly correlated with all behavioral measures: stage (R = −0.53, P < 0.01) (G), percent-correct response (R = −0.55, P < 0.001) (H), and running time (R = 0.61, P < 0.001) (I).