Distinct PFC and CA1 beta frequency activity after the reward location entry during spatial navigation tasks.

A. Spatial learning tasks on Y and F shaped mazes with spatial alternation rules. Animals were trained on the mazes across interleaved sessions. Reward locations (1, 2 and 3) are indicated. The order of visits required to ensure reward on every trial is shown above the maze schematics. The daily training schedule shows the duration, order and separation between sessions. B. Example PFC (orange) and CA1 (blue) LFP traces aligned to goal entry (black vertical line). Goal entry is the time when the animal reaches the reward delivery device at the end of each maze arm and breaks the infrared beam. This time is registered by an infrared sensor on the device. The beta frequency-filtered LFP is shown below the raw LFP. The heatmap shows the corresponding continuous wavelet transform spectrogram (<40 Hz). An extended frequency spectrogram is shown in Fig. 1-2. Beta bursts are indicated by horizontal lines. Dotted vertical lines mark 1 s intervals.C. PFC PSD (mean±sem) for time intervals when the animal is running on the maze (On Maze) (left) or is immobile at the goal (At Goal) (right). The aperiodic component shown in gray. An extended frequency version is shown in Fig. 1-3 D. CA1 power spectral density (mean±sem) for time intervals when the animal is running on the maze (left) or is immobile at the goal (right). The aperiodic component shown in gray. An extended frequency version is shown in Fig. 1-3. The peak marked by * in the CA1 PSD at ∼15 Hz corresponds to the first harmonic of theta (Scheffer-Teixeira & Tort, 2016). E. PFC PSDs with aperiodic component subtracted. F. CA1 PSDs with aperiodic component subtracted. The beta frequency range is shown in the inset. G. PFC difference between goal and maze PSDs (orange) with 95% confidence interval shown in gray. The beta frequency range is shown in the inset. H. CA1 difference between goal and maze PSDs (blue) with 95% confidence interval shown in gray. I. Frequency profile for beta bursts grouped by peak power frequency for PFC (orange) and CA1 (blue). Top: the vertical histogram of the mean frequency profiles for bursts at each peak power frequency. Bottom: histograms with the count distribution for bursts within 15-30 Hz, grouped by peak power frequency. Shading corresponds to the probability value at each frequency. Bursts occurring within 5 s after reward location entry are included. J. Cumulative distribution of peak burst frequencies for PFC (orange) and CA1 (blue). Kolmogorov-Smirnov test, p=2.9×10-103. K. Distribution of burst times relative to goal location entry grouped by peak frequency for PFC (orange) and CA1 (blue). L. Cumulative distribution of burst occurrence relative to goal location entry for PFC (orange) and CA1 (blue). Kolmogorov-Smirnov test, p=1.1×10-4.

Beta bursts occur independently in both regions.

A. Beta frequency bursts (shaded) detected across multiple electrodes in PFC (orange) and CA1 (blue) relative to reward location entry (black vertical line). The speed profile is shown in black. Three example trials are shown. B. Coherence (mean±SEM) within PFC (orange), between PFC and CA1 (green), or within CA1 (blue) for periods at the goal location. C. Mean coherence (15-30 Hz) across the groups. Pairwise rank sum test with Benjamini-Hochberg false discovery rate correction: p<0.001 for all pairs. D. Cross-correlation (mean±SD) of burst peak times for bursts detected on tetrodes within PFC (orange), across PFC-CA1 (green) and within CA1 (blue). E. Proportion of the cross-correlation density within ±50 ms lag for PFC (orange), across PFC-CA1 (green) and within CA1 (blue). Pairwise rank sum test with Benjamini-Hochberg false discovery rate correction: PFC versus PFC-CA1 (p=0.003**), PFC versus CA1 (p=0.24n.s.) and PFC-CA1 versus CA1 (p=0.003**). F. Frequency distribution of bursts by peak frequency for independent and coincident bursts in each region. G. Burst peak frequency distribution for coincident and independent bursts. Cumulative distribution burst occurrence relative to goal location entry. Kolmogorov-Smirnov test: PFC (p=0.96n.s.) and CA1 (p=0.002**).

Distinct changes in PFC and CA1 burst properties across days of learning.

A. Performance in each maze task by day. Linear model with fixed (day) and random (animal) effects. The marginal R2 (R2m) and conditional R2 (R2c) are shown. B. Burst power in each maze task by day. Linear model with fixed (day) and random (animal) effects. C. Performance in each maze task by performance quintile. Linear model with fixed (performance quintile) and random (animal) effects. D. Burst power in each maze task by performance quintile. Linear model with fixed (performance quintile) and random (animal) effects.

Bursts occur sooner after goal entry over days of training.

A. PFC burst delay distribution relative to goal entry versus days for unrewarded (left column) or rewarded (center column) trials, for the two maze tasks (top or bottom row), and their comparison (right column). B. CA1 burst delay distribution relative to goal entry versus days. C. PFC burst delay distribution relative to goal entry versus performance. D. CA1 burst delay distribution relative to goal entry versus performance.

PFC and CA1 cells show stronger spiking modulation to local beta.

A. Spike waveforms for example PFC cells. B. Spike waveforms for example CA1 cells. C. Spike triggered power spectrum for example PFC cells. D. Spike triggered power spectrum for example CA1 cells. E. Spike beta phase-locking raster and histogram for example PFC cells. Spike raster is arranged by trial and goal location (color shading). The corresponding mean histogram for each goal location is shown below. The phase of beta is shown in gray. F. Spike beta phase-locking raster and histogram for example CA1 cells. G. Goal location-aligned spiking raster for the example PFC cells. The mean firing rate for each goal location is shown below the spike raster. The corresponding speed at each goal is in the lower row. H. Goal location-aligned spiking raster for the example CA1 cells. I. Distribution of Rayleigh z for PFC. J. Distribution of k from a von Mises distribution fit for significantly beta-modulated cells (Rayleigh p <0.05 in panel b) in PFC. K. Distribution of phase preference for significantly beta-modulated cells in PFC. Red dotted line shows the mean population phase preference. The gray line indicates the phase of beta. L. Distribution of Rayleigh z for CA1. M. Distribution of k from a von Mises distribution fit for significantly beta-modulated cells (Rayleigh p <0.05 in panel b) in CA1. N. Distribution of phase preference for significantly beta-modulated cells in CA1 O. PFC beta phase locking strength using the Rayleigh test (Rayleigh z) to PFC or CA1 beta. Wilcoxon signed-rank test: p=5.4×10-50. P. PFC beta phase locking strength using the von Mises fit (kappa) to PFC or CA1 beta. Wilcoxon signed-rank test: p=5.6×10-43. Q. CA1 beta phase locking strength using the Rayleigh test (Rayleigh z) to CA1 or PFC beta. Wilcoxon signed-rank test: p=5.3×10-55. R. Beta phase locking strength using the von Mises fit (kappa) to CA1 or PFC beta. Wilcoxon signed-rank test: p=1.5×10-45 S. Goal location classification based on mean phase preference at each goal (schematic on the left). Bar plot shows the proportion of the PFC population (non-beta or beta-modulated) that distinguished goal identity based on mean phase preference at each goal. Fisher’s exact test: p=0.19. T. Goal location classification based on mean firing rate each goal (schematic on the left). Bar plot shows the proportion of the PFC population (non-beta or beta-modulated) that distinguished goal identity based on mean firing rate at each goal. Fisher’s exact test: p=0.042. U. Bar plot shows the proportion of the CA1 population (non-beta or beta-modulated) that distinguished goal identity based on mean phase preference at each goal. Fisher’s exact test: p=0.70. V. Bar plot shows the proportion of the CA1 population (non-beta or beta-modulated) that distinguished goal identity based on mean firing rate at each goal. Fisher’s exact test: p=0.66. W. Mean spiking speed for PFC cells based on beta modulation. Wilcoxon rank sum test: p=0.41. X. Spiking distance to nearest goal for PFC cells based on beta modulation. Wilcoxon rank sum test: p=0.0006. Y. Spatial information for PFC cells based on beta modulation. Wilcoxon rank sum test: p=0.18. Z. Mean spiking speed for CA1 cells based on beta modulation. Wilcoxon rank sum test: p=0.29 AA. Spiking distance to nearest goal for CA1 cells based on beta modulation. Wilcoxon rank sum test: p=0.13 BB. Spatial information for CA1 cells based on beta modulation. Wilcoxon rank sum test: p=0.013.

Goal location beta bursts and SWRs are coordinated at multiple timescales.

A. PFC (orange) and CA1 (blue) LFP relative to goal entry (black vertical line). Beta frequency filtered signal is shown below the LFP. Ripple frequency (150-250 Hz) filtered CA1 signal is shown in black. The corresponding speed of the animal is shown in the bottom row. B. Goal-entry-aligned histogram for CA1 SWRs. Median and interquartile range are shown. C. Goal-entry-aligned histogram for PFC beta bursts. D. Goal-entry-aligned histogram for CA1 beta bursts. E. Cross-correlation between PFC beta bursts and CA1 SWRs (±5 s, 1 s bins). Wilcoxon signed-rank test p=5.2×10-8. F. Cross-correlation between CA1 beta bursts and CA1 SWRs (±5 s, 1 s bins). Wilcoxon signed-rank test p=7.1×10-8. G. Cross-correlation between PFC beta bursts and CA1 SWRs (±500 ms, 100 ms bins). Bins with significant deviations (with Benjamini-Hochberg false discovery rate correction) from the mean are indicated with *. H. Cross-correlation between CA1 beta bursts and CA1 SWRs (±500 ms, 100 ms bins). Bins with significant deviations (with Benjamini-Hochberg false discovery rate correction) from the mean are indicated with *. I. SWR-aligned PFC spectrogram (100-300 Hz) and corresponding ripple band power (150-250 Hz). J. SWR-aligned CA1 spectrogram (100-300 Hz) and corresponding ripple band power (150-250 Hz). K. SWR-aligned PFC spectrogram (10-30 Hz) and corresponding beta-band power (15-30 Hz). L. SWR-aligned CA1 spectrogram (10-30 Hz) and corresponding beta-band power (15-30 Hz).

SWR and beta modulation in PFC and CA1.

A. Four example PFC cells showing SWR-aligned spiking raster and histogram, and spike beta-phase-locking histogram. Top two cells show spiking excitation around SWRs, and bottom two cells show spiking inhibition around SWRs. The SWR modulation index (MI) is displayed. In the spike beta-phase-locking histogram, the distribution is duplicated to improve visualization. The peaks and troughs for the beta cycle are shown in white and the phase locking strength (k) is displayed. B. PFC beta modulation strength (kappa) versus SWR modulation index. The four combinations of SWR (S) and beta (β) modulation (+: modulated and -: not modulated) and their corresponding proportions are indicated. C. PFC SWR modulation index versus beta phase locking preference for beta and SWR-modulated cells (β+S+) (upper) and beta-modulated but not SWR-modulated cells (β-S+) (lower). The regression line is shown in cyan. The gray shading indicates the peak and trough of beta. Two cycles are repeated for clarity. D. Spiking distance to nearest goal versus SWR modulation index. E. Spiking speed versus SWR modulation index. F. Spatial information versus SWR modulation index. G. Four example CA1 cells showing SWR-aligned spiking raster and histogram and spike beta-phase-locking histogram. H. CA1 beta modulation strength (kappa) versus SWR modulation index. The four combinations of SWR and beta (β) modulation (+: modulated and -: not modulated) and their corresponding proportions are indicated. I. CA1 SWR modulation index versus beta phase locking preference for beta and SWR-modulated cells (β+S+) (upper) and SWR-modulated but not beta-modulated cells (β-S+) (lower). The regression line is shown in red. The gray shading indicates the peak and trough of beta. Two cycles are repeated for clarity. J. Spiking distance to nearest goal versus SWR modulation index. K. Spiking speed versus SWR modulation index. L. Spatial information versus SWR modulation index.

Location of recording tetrodes.

A. Representative histology showing location of tetrodes in PFC. B. Representative histology showing location of tetrodes in CA1.

Extended frequency spectrogram for example goal-aligned PFC and CA1 LFP.

Same example as Fig. 1B with spectrogram up to 100 Hz.

Power spectral density by brain region, frequency band and maze task

A. Average across both Y and F mazes. Periodic PSD component for PFC (orange) and CA1 (blue) for periods when the animal is running on the maze or immobile at the goal. Each column corresponds to a specific frequency range (marked above each plot) to display the appropriate power range. The sharp peak at 60 Hz corresponds to line noise.B. Average across both Y and F mazes. Difference between goal and maze periodic PSDs with 95% confidence interval shown in gray. C. Y maze only. Periodic PSD component for PFC (orange) and CA1 (blue). Same format as A. D. Y maze only. Difference between goal and maze periodic PSDs with 95% confidence interval shown in gray. E. F maze only. Periodic PSD component for PFC (orange) and CA1 (blue). Same format as A. F. F maze only. Difference between goal and maze periodic PSDs with 95% confidence interval shown in gray.

Goal-entry-aligned spectrogram.

A. PFC spectrogram for all maze task sessions (left), Y maze (center) or F maze (right). Spectrogram generated using continuous wavelet transform. Session count shown in Table 1-1. B. CA1 spectrogram. C. Corresponding goal-entry-aligned speed profile (mean±std). D. Mean PFC power for 3 s before (maze) or after goal entry (goal). E. Difference in PFC power for 3 s before (maze) or after goal entry (goal). 95% confidence interval shown in gray. F. Mean CA1 power for 3 s before (maze) or after goal entry (goal). G. Difference in CA1 power for 3 s before (maze) or after goal entry (goal). 95% confidence interval shown in gray.

Burst detection.

A. Two example bursts with corresponding LFP and continuous wavelet transform from PFC (1.5 s each, top row). The burst is marked by the black horizontal line. The corresponding continuous wavelet transform is shown in the middle row. The white cross marks the frequency and time corresponding to the maximum power in the burst interval. The mean power in the beta band (15-30 Hz) from the continuous wavelet transform is shown by the histogram in the bottom row. The solid black line corresponds to 1 standard deviation (z) above the mean (1z), and the dotted black line corresponds to 0.5 standard deviation above the mean (0.5z). To detect bursts, we identify intervals during which the beta-band power exceeds 0.5 standard deviation above the mean. Intervals are included if the maximum power in the interval exceeds 1 standard deviation above the mean, and the duration of the interval is greater than 100 ms. Intervals separated by less than 100 ms were merged. The peak frequency for each burst is the frequency corresponding to the maximum power within the burst interval. B. Two example bursts from CA1.

Power and duration for beta bursts by frequency.

A. Beta burst power by peak burst frequency. B. Beta bursts duration by peak burst frequency.

Session count.

*Day 5 for animal 2 was excluded due to noise in the recording.

Tetrode count.

Coherence and burst coincidence within and across each hemisphere.

A. Coherence within left PFC (mean±SEM). B. Coherence within right PFC (mean±SEM). C. Coherence between left and right PFC (mean±SEM). D. Beta frequency coherence within each and across both PFC hemispheres. Each data point is the mean of each experiment day. E. Coherence between ipsilateral PFC and CA1. F. Coherence between contralateral PFC and CA1. G. Beta frequency coherence for ipsi- and contralateral PFC and CA1. H. Cross-correlation (mean±SD) of burst peak times for bursts detected on tetrodes with left PFC. I. Cross-correlation (mean±SD) of burst peak times for bursts detected on tetrodes with right PFC. J. Cross-correlation (mean±SD) of burst peak times for bursts detected between left and right PFC. K. Proportion of the cross-correlation density within ±50 ms lag for left, right and across PFC hemisphere. L. Cro ss-correlation (mean±SD) of burst peak times for bursts detected between ipsilateral PFC and CA1. M. Cross-correlation (mean±SD) of burst peak times for bursts detected between contralateral PFC and CA1. N. Proportion of the cross-correlation density within ±50 ms lag for ipsi- and contralateral PFC and CA1.

Beta burst-aligned power and coherence

a. Multi-taper power spectrum within a 1 s window centered on the peaks of independent or coincident beta bursts (columns) in the PFC (top row) and CA1 (bottom row). The heatmap shows the mean across all bursts in each category. b. Power (18-25 Hz) within ±100 ms of the peak. PFC (orange, top) and CA1 (blue, bottom). Pairwise rank-sum test with Benjamini-Hochberg false discovery rate correction: p<0.001*** and p<0.05* for all significant comparisons. c. Change in power within ±100 ms of the peak relative to baseline (125 ms from - 0.5 s). PFC (orange, top) and CA1 (blue, bottom). Wilcoxon signed-rank test with Benjamini-Hochberg false discovery rate correction: p<0.001***. d. Multi-taper coherence in PFC (upper row) and CA1 (lower row) within a 1 s window centered on the peaks of independent or coincident beta bursts. The heatmap shows the mean across all bursts in each category. e. Coherence (18-25 Hz) within ±100 ms of the peak in PFC (upper row) and CA1 (lower row). Pairwise rank sum test with Benjamini-Hochberg false discovery rate correction: p<0.001*** and p<0.05* for all significant comparisons. f. Change in coherence within ±100 ms of the peak relative to baseline (125 ms from −0.5 s). PFC (orange, top) and CA1 (blue, bottom). Wilcoxon signed-rank test with Benjamini-Hochberg false discovery rate correction: p<0.001***. g. PFC-CA1 coherence within a 1 s window centered on the peaks of independent or coincident beta bursts. The heatmap shows the mean across all bursts in each category. h. PFC-CA1 coherence between (18-25 Hz) within ±100 ms of the peak in PFC (top row) and CA1 (bottom row). Pairwise rank sum test with Benjamini-Hochberg false discovery rate correction: p<0.001*** and p<0.01** for all significant comparisons. i. Change in PFC-CA1 coherence within ±100 ms of the peak relative to baseline (125 ms from - 0.5 s). PFC (orange, top) and CA1 (blue, bottom). Wilcoxon signed-rank test with Benjamini-Hochberg false discovery rate correction: p<0.001*** and p<0.01**.

Session summary.

Animal speed at the time of bursts.

A. PFC bursts in Y maze task by day. B. PFC bursts in Y maze task by performance. C. CA1 bursts in Y maze task by day. D. CA1 bursts in Y maze task by performance. E. PFC bursts in F maze task by day. F. PFC bursts in F maze task by performance. G. CA1 bursts in F maze task by day. H. CA1 bursts in F maze task by performance.

Beta coherence within and across brain regions by experiment day by maze.

A. PFC coherence by day in the Y maze task. B. PFC-CA1 coherence by day in the Y maze task. C. CA1 coherence by day in the Y maze task D. PFC coherence by day in the F maze task. E. PFC-CA1 coherence by day in the F maze task. F. CA1 coherence by day in the F maze task. G. PFC coherence by performance in the Y maze task H. PFC-CA1 coherence by performance in the Y maze task. I. CA1 coherence by performance in the Y maze task. J. PFC coherence by performance in the F maze task. K. PFC-CA1 coherence by performance in the F maze task. L. CA1 coherence by performance in the F maze task.

Beta burst coincidence within and across brain regions by experiment day by maze

A. PFC burst coincidence by day in the Y maze task. Value shows the proportion of the cross-correlation density within ±50 ms lag, similar to Fig. 2E. B. PFC-CA1 burst coincidence by day in the Y maze task. C. CA1 burst coincidence by day in the Y maze task. D. PFC burst coincidence by day in the F maze task. E. PFC-CA1 burst coincidence by day in the F maze task. F. CA1 burst coincidence by day in the F maze task. G. PFC burst coincidence by performance in the Y maze task. H. PFC-CA1 burst coincidence by performance in the Y maze task. I. CA1 burst coincidence by performance in the Y maze task. J. PFC burst coincidence by performance in the F maze task. K. PFC-CA1 burst coincidence by performance in the F maze task. L. CA1 burst coincidence by performance in the F maze task.

Animal speed at the time of bursts.

A. PFC (orange) and CA1 (blue) bursts in Y maze task versus day for unrewarded or rewarded trials. B. PFC (orange) and CA1 (blue) bursts in F maze task versus day for unrewarded or rewarded trials. C. PFC (orange) and CA1 (blue) bursts in Y maze task versus performance for unrewarded or rewarded trials. D. PFC (orange) and CA1 (blue) bursts in F maze task versus performance for unrewarded or rewarded trials.

Burst delay by maze for unrewarded and rewarded trials.

A. PFC burst delay by day (Fig. 4A). B. CA1 bursts delay by day (Fig. 4B). C. PFC bursts delay by performance (Fig. 4C). D. CA1 bursts delay by performance (Fig. 4D).

Burst frequency for unrewarded and rewarded trials.

A. PFC (upper) and CA1 (lower) burst frequency for both maze tasks. B. PFC (upper) and CA1 (lower) burst frequency for Y maze tasks. C. PFC (upper) and CA1 (lower) burst frequency for F maze tasks.

Permutation test for frequency variance across days.

A. Burst peak frequency variance in each maze task by day. Linear model with fixed (day) and random (animal) effects. B. Permutation test for the slope of regression in A. Solid line shows the observed slope. Gray histogram shows the permuted distribution where the experiment day identity was shuffled (n=1000). C. Burst peak frequency variance in each maze task by performance quintile. Linear model with fixed (performance quintile) and random (animal) effects. D. Permutation test for the slope of regression in C. Solid line shows the observed slope. Gray histogram shows the permuted distribution where the performance percentile was shuffled (n=1000).

Beta phase locking by maze task.

A. Distribution of Rayleigh z for PFC. B. Distribution of k from a von Mises distribution fit for significantly beta-modulated cells (Rayleigh p <0.05 in panel b) in PFC. C. Distribution of phase preference for significantly beta-modulated cells in PFC. Red dotted line shows the mean population phase preference. The gray line indicates the peak and trough of beta. D. Distribution of Rayleigh z for CA1. E. Distribution of k from a von Mises distribution fit for significantly beta-modulated cells (Rayleigh p <0.05 in panel b) in CA1. F. Distribution of phase preference for significantly beta-modulated cells in CA1. Red dotted line shows the mean population phase preference. The gray line indicates the peak and trough of beta.

Spiking task correlates by maze task.

A. Mean spiking speed for PFC and CA1 cells based on beta modulation. B. Spiking distance to nearest goal for PFC and CA1 cells based on beta modulation. C. Spatial information for PFC and CA1 cells based on beta modulation.

Cell type classification.

Cell count per day.

Cell count by maze.

Cell count by beta phase locking.

CA1 SWR properties versus day by maze task.

A. SWR power. B. SWR rate. C. SWR duration. D. Animal speed during SWR. E. Goal period count per animal. F. Goal period duration.

SWR-aligned spectrogram by maze task.

A. SWR-aligned PFC spectrogram (100-300 Hz) and corresponding ripple band power (150-250 Hz). B. SWR-aligned PFC spectrogram (10-30 Hz) and corresponding beta-band power (15-30 Hz). C. SWR-aligned CA1 spectrogram (100-300 Hz) and corresponding ripple band power (150-250 Hz). D. SWR-aligned CA1 spectrogram (10-30 Hz) and corresponding beta-band power (15-30 Hz).

Phase amplitude coupling between SWR band power and beta phase during SWRs.

A. Y maze SWR band power relative to PFC beta phase. The normalized mean SWR band power (z) across all sessions is shown in blue. The 99% confidence interval from a circular permutation test (5000 shuffles) is shown in gray. The permutation test circularly permutes the phase value for each session. B. F maze SWR band power relative to PFC beta phase. C. Y maze SWR band power relative to CA1 beta phase. SWR band power showed significant deviation from the shuffle bounds around the peak of beta. D. F maze SWR band power relative to CA1 beta phase. SWR band power showed significant deviation from the shuffle bounds around the peak of beta.

Permutation test for the significance of the correlation coefficient.

A. Distribution of the permuted (gray) and observed (vertical line) for PFC SWR modulation index versus beta phase locking preference in Fig. 7C. We performed this additional permutation test to verify that the observed value of the correlation coefficient is different from the chance distribution. B. Distribution of the permuted (gray) and observed (vertical line) for CA1 SWR modulation index versus beta phase locking preference in Fig. 7I.

Task correlates by beta and SWR modulation.

A. Proportion of each PFC (left two columns) and CA1 (right two columns) population that distinguishes goal identity based on phase preference at each goal. B. Proportion of each PFC and CA1 population that distinguishes goal identity based on mean firing rate at each goal.