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Phase-tuned neuronal firing encodes human contextual representations for navigational goals

  1. Andrew J Watrous  Is a corresponding author
  2. Jonathan Miller
  3. Salman E Qasim
  4. Itzhak Fried
  5. Joshua Jacobs  Is a corresponding author
  1. Columbia University, United States
  2. Dell Medical School, University of Texas at Austin, United States
  3. Seton Brain and Spine Institute, United States
  4. David Geffen School of Medicine, University of California, Los Angeles, United States
  5. University of California, Los Angeles, United States
  6. Tel-Aviv University, Israel
  7. Tel-Aviv Medical Center, Israel
Research Advance
Cite this article as: eLife 2018;7:e32554 doi: 10.7554/eLife.32554
4 figures, 1 data set and 1 additional file

Figures

Figure 1 with 1 supplement
Firing rate modulations by navigational goal and task phase.

(A) Neuron from the entorhinal cortex of patient four whose firing rate was significantly goal-modulated when delivering to goal 3 (p<0.001). Firing rate is plotted as a function of each navigational goal (error bars indicate s.e.m.). (B) Proportion of goal-responsive neurons in each brain area. Asterisk indicates significant counts using binomial test. (C) Example neuron from the hippocampus of patient 12 whose firing rate was modulated during goal planning (p<0.0001). (D) Example neuron from the parahippocampal gyrus of patient eight whose firing rate was modulated during goal arrival (p=0.0002). (E) Proportion of task-responsive neurons in each brain area, shown separately for planning and arrival. See methods for region acronyms.

https://doi.org/10.7554/eLife.32554.002
Figure 1—figure supplement 1
Task and recording methods.

(A) Overhead view of the virtual environment. Goal stores are outlined in red. (B) Microelectrode bundle from the right entorhinal cortex of patient #2. (C) Example spike waveforms for neurons isolated from the bundle shown in B.

https://doi.org/10.7554/eLife.32554.003
Figure 2 with 2 supplements
Multiple Oscillation Detection Algorithm (‘MODAL’).

(A-C) Key steps in the algorithm, shown for an example electrode from the right hippocampus of patient 9. (A) Mean log power averaged over time (black) and a fit line of the 1/f background spectrum (gray). A slow theta band (blue) and a beta band (green) are identified as contiguous frequencies exceeding the fit line. (B) Example output from MODAL depicting a raw trace example of the LFP (upper) with the detected oscillations in each band (lower). The instantaneous frequency of the detected oscillation in each band is overlaid on a spectrogram and gray portions of the spectrogram indicate power values exceeding a local fit (similar to A but using a 10 s epoch). (C) Accumulating detections over time reveals the prevalence of oscillations at each frequency on this electrode (black). Blue and green bars indicate the overall prevalence of oscillations in each frequency, independent of the exact frequency within a band. (D) Population data for MTL channels demonstrating low frequency oscillations. Grey line indicates the percent of LFP channels with a detected band as a function of frequency. Of those channels with a detected band, the black line indicates the average amount of time each frequency was detected. Slow theta oscillations (below 5 Hz) are observed using both metrics.

https://doi.org/10.7554/eLife.32554.004
Figure 2—figure supplement 1
Proportion of channels with oscillations detected using MODAL in each brain region.
https://doi.org/10.7554/eLife.32554.005
Figure 2—figure supplement 2
Analysis of rodent CA1 and medial prefrontal cortex LFPs using MODAL.

Analysis of rodent medial prefrontal cortex (A) and hippocampal CA1 (B) recordings using MODAL. Data provided by Fujisawa and taken from crcns.org (PFC-2 dataset). The first five minutes of recordings from one rat (EE) were analyzed. Upper panels show example raw traces.

https://doi.org/10.7554/eLife.32554.006
Phase-Locked Neural Firing to low-frequency oscillations.

(A) Spike-triggered average of a phase-locked neuron from the right hippocampus of Patient 1 (left). Red tick mark denotes a spike. Circular histograms (right) show phases at which spikes occurred relative to two detected bands. Spiking was phase-locked to the ascending phase in the 1.5–5 Hz band (red) but not in the 7.5–9 Hz band (Rayleigh test, p=0.004 and p=0.34, respectively). (B) MTL Population data: Pooling over frequencies, mean spike phases were significantly clustered near the initial ascending phase of the oscillation (Rayleigh test, p<0.00001). (C) Population scatter plot of the mean phase of firing and maximally detected frequency within the band for each phase-locked MTL neurons. (D) Population results showing proportion of phase-locked neurons in each brain region. Total bar height indicates the proportion of neurons recorded on an LFP channel with a band in the 1–10 Hz range. See methods for region acronyms.

https://doi.org/10.7554/eLife.32554.007
Figure 4 with 2 supplements
Spike–Phase coding for navigational goals.

(A) Example neuron from the right hippocampus of patient one showing significant spike-LFP phase coding for goal four compared to goals 5 and 6. Circular histograms show spike counts separately for different goals. Black line at center of each plot shows the resultant vector and the colored arc indicates the 95th percentile confidence interval of the circular mean. (B) Example cell from left entorhinal cortex of patient six showing phase coding for goal 6. (C) Population summary showing the proportion of significant neurons in each region that showed rate coding, phase coding, or both effects. Pooling over regions, we observed significant phase coding in 10% of cells. LEC: Left entorhinal cortex; RH: Right hippocampus.

https://doi.org/10.7554/eLife.32554.008
Figure 4—figure supplement 1
Single-trial examples of phase coding in Patient 1. 

(A-F) Example of a phase-coding neuron from the right hippocampus of Patient 1. This neuron showed significant decoding using spike phases (shuffle corrected p=0.002) and no firing rate effects (all p>0.5 using two-way ANOVA with goal and task period). Phase coding was more robust during goal arrival than during planning (p<0.002 and p=0.08, respectively) and is evident when comparing panel C and F. (A) LFP traces and spiking for a single delivery to goal 2, demonstrating consistent spiking near the ascending peak of the low-frequency oscillation (MODAL band detected 1–5 Hz oscillations). Inset in A shows the spike waveform of the neuron. Colored tick marks indicate spikes during oscillations using MODAL and are color-coded by instantaneous phase (color scheme seen in S4B). (B–C) Normalized spike phase histograms for goal store two deliveries across all deliveries during planning periods (B) and arrival periods (C). Black lines in center indicate resultant vector length and black arc outside of circle indicates circular 95th percentile confidence intervals. Absence of this black arc indicates lack of significant phase locking for the distribution (Rayleigh p>0.05). (D–F) Similar to A-C but for a delivery to goal 5. Spike phases occur near the trough of the oscillation upon arrival at the goal.

https://doi.org/10.7554/eLife.32554.009
Figure 4—figure supplement 2
Single-trial examples of data from a neuron in Patient 11.

(A-D) Examples of rate and phase-coding by a neuron from the left hippocampus of patient 11. This neuron showed significant rate coding for goal 3 (panel E) and phase-coding during arrival at goal 1 (p=0.028, panel D). (A) LFP traces and spiking for a single delivery to goal 3, demonstrating spiking at random phases of the low-frequency oscillation (MODAL band detected 1–6.5 Hz oscillations). Colored tick marks indicate spikes during oscillations using MODAL and are color-coded by instantaneous phase (color scheme seen in 4C). Grey ticks indicate spikes during non-oscillatory periods. (C–D) Normalized spike phase histograms for each goal that demonstrated phase-locking during planning periods (C) and arrival periods (D). Colored lines in center indicate resultant vector length and arcs outside of circle indicates circular 95th percentile confidence intervals. Absence of this arc (e.g. for goal 3) indicates lack of significant phase locking for the distribution (Rayleigh p>0.05). (E) Firing rate for each goal, demonstrating that this neuron showed elevated firing for goal three deliveries (p<0.009).

https://doi.org/10.7554/eLife.32554.010

Data availability

The raw data can be obtained upon request from Joshua Jacobs (joshua.jacobs@columbia.edu). At this point, the raw data have not been made publicly available to ensure controlled access to the dataset and that the patients' anonymity is not compromised.

The following previously published data sets were used
  1. 1

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