Research ArticleNEUROPHYSIOLOGY

Multiplexed oscillations and phase rate coding in the basal forebrain

See allHide authors and affiliations

Science Advances  01 Aug 2018:
Vol. 4, no. 8, eaar3230
DOI: 10.1126/sciadv.aar3230
  • Fig. 1 Beta, gamma, and hi-gamma transients occur within a temporal framework that is referenced to theta.

    (A) Average power spectral density plots for 36 recordings from four animals. Dark and light transparent shadings represent 1 and 2 SDs, respectively. We calculated the plots using LFP data from the entire recording sessions (~25 to 40 min). Power spectral density plots were also remarkably consistent across recording days in single individuals (fig. S2A). (B) Example of 2-s raw LFP trace (black), and z-scored power at theta (gray; 4 to 9 Hz), beta (orange; 20 to 35 Hz), gamma (blue; 45 to 65 Hz), and hi-gamma (magenta; 80 to 150 Hz) frequency bands. (C) Average power/power correlations for all animals across all frequencies, showing that there are multiple frequency bands that are correlated within a given range but independent from other frequency ranges. Color axis, 0 to 0.5. (D) Phase/amplitude coupling to theta (4 to 9 Hz) frequency. We plotted the average theta wave, aligned by the peaks, across all recordings as the gray line. The colormap represents the average wavelet transform relative to the peak of theta. Beta (20 to 35 Hz) and hi-gamma (80 to 150 Hz) frequencies increase in amplitude during troughs in theta, while gamma power (45 to 60 Hz) increases at the peak of theta oscillations. Orange, blue, and magenta ticks on the average theta wave indicate maximum power for beta, gamma, and hi-gamma frequency bands, respectively. Black vertical bar for theta wave, −2 to +2 μV. Values at each frequency are normalized to the highest value at the same frequency. Color axis, 0 to 1.

  • Fig. 2 Individual BF neurons phase-lock to specific frequency bands.

    (A) For each example neuron (columns), there are four plots (rows) that show the spike time histograms relative to the phase of theta, beta, gamma, and hi-gamma oscillations. Colored boxes map onto the colored dots in (B). (B) For each neuron, we calculated resultant vectors for the distribution of phase angles at spike times and for randomized spike times (average of 100 iterations). Scatterplots depict the actual resultant vector (y axis) and the average resultant vector with randomized spike times (x axis) for each neuron. Red lines indicate a slope of 1, and colored dots map onto the colored outlines in (A). Light green, blue, teal, and yellow dots correspond to strongly phase-locked neurons for theta, beta, gamma, and hi-gamma, respectively; while magenta, orange, red, and dark green dots correspond to neurons with weak or no modulation for theta, beta, gamma, and hi-gamma, respectively. (C) For each neuron, we then used Rayleigh’s test for nonuniformity to determine whether spike times were uniformly distributed or locked to particular phases of theta, beta, gamma, or hi-gamma oscillations. The proportion of neurons with P < 0.05 is represented as the black dots for each frequency band. The mean proportion of neurons with P < 0.05 when spike times are randomly shuffled (100 iterations; error bars are ±3 SDs) is shown in red. (D) The proportion of neurons with significantly nonuniform spike phase distributions for one, two, three, or four of the observed frequency bands is shown as black dots. The proportion of neurons with P < 0.05 for one, two, three, or four frequency bands when spike times are randomly shuffled (100 iterations; error bars are ±3 SDs) is shown in red.

  • Fig. 3 Neuronal firing is correlated with the oscillation amplitude of specific frequency bands.

    (A) Example tracking data from a single trial (left) and 24 recordings (right). We detected the head location via two head-mounted light-emitting diodes (LEDs) (black dots). Green, cyan, magenta, and red dots indicate the head location during the light flash, nosepoke, plate cross, and reward location, respectively. (B) Example spike trains from 45 simultaneously recorded BF neurons across a single trial. (C) Raw LFP trace from the same example trial as in Fig. 2B. (D) Wavelet transform of LFP trace in Fig. 2C. Note the gamma and beta transients after the light flash and nosepoke, respectively (color axis, 0 to 1; maximum normalization performed individually for each frequency bin). (E) Left: Average wavelet transform of LFPs recorded during the selective attention task. Changes in LFP power during the task can be observed across all four frequencies: theta (4 to 9 Hz), beta (20 to 35 Hz), gamma (45 to 60 Hz), and hi-gamma (80 to 150 Hz). All frequencies (rows) are individually maximum-normalized (color axis, 0 to 1) to visualize changes across the spectrum of frequencies present. Right: Proportion (color axis, 0 to 1) of recordings with LFP power fluctuations that were significantly different from equal length segments randomly selected from the recording for all frequencies (1 to 150 Hz) and task epochs (1 to 540 Hz). Note that both significant increases and decreases (hi-gamma during return) in power are observed during specific task epochs. KS tests thresholded at P < 0.05. (F) Left: Mean firing rates for 780 BF neurons. Each row is the average firing rate (~70 trials) for a single neuron; the population is sorted by the point of maximum firing during the selective attention task (color axis, 0 to 1; with each maximum normalization performed individually for each row/neuron). Right: Neurons with specific firing patterns, relative to epochs of the selective attention task, correlate with specific frequency bands in the LFP (left). For each trial, we correlated the cross-epoch firing rate vector for each neuron (Pearson’s product-moment correlation) with the wavelet transform of the LFP across the same epochs. These correlations are then averaged across trials, generating a matrix where the y axis is the neuron number (1 to 780) and the x axis is the LFP frequency (1 to 150 Hz). The rows of this correlation matrix are then sorted to match the order of (E), maximum-normalized, and smoothed with the nearest 30 neurons (moving window along the y axis; color axis is between 0 and 1). For comparison with correlation values expected by chance, see fig. S4. Black vertical lines [across (E) and (F)] mark the light flash, nosepoke, plate cross, and reward, while the black horizontal lines [across (E) and (F)] mark the neurons with peak firing rates closest to these behaviorally defined events.

  • Fig. 4 BF neurons theta phase precess across task epochs.

    (A) Scatterplots, for five example cells, of spike times relative to LFP theta phase (y axis) and task epoch (x axis). To aid visualization, theta cycles are repeated three times on the y axis, and colored arrows depict behavioral events on the x axis (green, light; cyan, nosepoke; magenta, plate cross; red, reward). Above the scatterplots, blue lines represent the average firing rate for each neuron across the selective attention task (normalized to maximum rate; y axis is 0 to 1). (B) Spike density heat maps of the data given in Fig. 3A. (C) Theta phases are uniformly distributed across task epochs. Circular SDs of theta phases are plotted in black, and those expected by chance are plotted in red (10× shuffled; bounded line is a 99% confidence interval). Green dots depict the few task epochs with nonuniform theta phase distributions. (D) Example cell #3 is depicted again with circular-linear correlations plotted as the slope for each of its firing fields (epochs 1 to 138, 185 to 251, and 291 to 502) (see Materials and Methods for firing field definition). Note that its second and third firing fields display strong circular/linear correlations between theta phase and task epoch. (E) Proportion of neurons that are active (>50% maximum firing rate) and also exhibiting significant phase precession as a function of task epoch. For each task epoch (x axis), all significant theta precessing firing fields with centers of mass within ±10 epochs were summed (y axis). Gray line indicates precession relative to 4- to 9-Hz theta. Orange, blue, and magenta lines indicate precession relative to beta, gamma, and hi-gamma, respectively. Red line indicates the proportion of neurons expected by chance to be precessing at each task epoch relative to 4- to 9-Hz theta.

  • Fig. 5 BF phase precession is relative to task epoch progression, not absolute time or spatial location.

    (A) For each neuron, we compared the firing field with the maximum circular linear correlation (y axis) with the average circular linear correlation when theta epochs were randomly shuffled across spike times (mean of 100 iterations; x axis). Circular/linear correlations are consistently larger for actual task phase precession than for theta phase shuffled data. Green dots indicate neurons with P < 0.05 for a one-sample t test between actual and shuffled data (123 of 780 neurons) (B) Rather than task epochs as in Fig. 5A, we used absolute time relative to trial onset as the linear variable for precession (see fig. S6 for example neurons). Green dots indicate neurons with P < 0.05 for a one-sample t test between actual and shuffled data (84 of 780 neurons). (C) Rather than task epochs as in Fig. 5A, we used cumulative distance traveled from the trial start as the linear variable to test for phase precession (see fig. S6 for example neurons). Cumulative distance was calculated as the summed Euclidean distance between each position tracking frame from the start of the trial to the frame at which a spike occurred. Green dots indicate neurons with P < 0.05 for a one-sample t test between actual and shuffled data (89 of 780 neurons).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/4/8/eaar3230/DC1

    Fig. S1. Summary of LFP and multiple single-neuron recording sites in BF.

    Fig. S2. Theta, beta, gamma, and hi-gamma frequencies are observed across multiple recording days and animals.

    Fig. S3. Average wavelet transform of LFPs during selective attention task.

    Fig. S4. Firing rate/LFP correlation control.

    Fig. S5. Cross-correlogram offsets for simultaneously recorded neuron pairs correlate with distance between task epochs associated with maximal firing.

    Fig. S6. BF neuron theta phase precession relative to task epoch, time, and space.

    Table S1. Phase-locking strengths do not correlate with burstiness or firing rate.

    Table S2. Phase-locking resultants do not correlate with task phase–specific firing or power/rate correlations.

  • Supplementary Materials

    This PDF file includes:

    • Fig. S1. Summary of LFP and multiple single-neuron recording sites in BF.
    • Fig. S2. Theta, beta, gamma, and hi-gamma frequencies are observed across multiple recording days and animals.
    • Fig. S3. Average wavelet transform of LFPs during selective attention task.
    • Fig. S4. Firing rate/LFP correlation control.
    • Fig. S5. Cross-correlogram offsets for simultaneously recorded neuron pairs correlate with distance between task epochs associated with maximal firing.
    • Fig. S6. BF neuron theta phase precession relative to task epoch, time, and space.
    • Table S1. Phase-locking strengths do not correlate with burstiness or firing rate.
    • Table S2. Phase-locking resultants do not correlate with task phase–specific firing or power/rate correlations.

    Download PDF

    Files in this Data Supplement:

Navigate This Article