Ripples reflect a spectrum of synchronous spiking activity in human anterior temporal lobe

  1. Ai Phuong S Tong
  2. Alex P Vaz
  3. John H Wittig
  4. Sara K Inati
  5. Kareem A Zaghloul  Is a corresponding author
  1. Surgical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, United States
  2. Medical Scientist Training Program, Duke University School of Medicine, United States
  3. Office of the Clinical Director, National Institute of Neurological Disorders and Stroke, National Institutes of Health, United States
4 figures and 2 additional files

Figures

Figure 1 with 6 supplements
High-frequency activity reflects discrete ripples.

(A) Paired-associates verbal episodic memory task. (B) Average iEEG signal locked to detected ripples in an anterior temporal lobe electrode in two participants. (C) Time-frequency power …

Figure 1—source code 1

Matlab code of ripple events in the iEEG signal.

https://cdn.elifesciences.org/articles/68401/elife-68401-fig1-code1-v2.zip
Figure 1—figure supplement 1
Ripple-triggered average iEEG and LFP signals.

(A) Average intracranial EEG (iEEG) signal locked to each ripple detected in the anterior temporal lobe iEEG electrodes in each session across six participants. (B) Average local field potential …

Figure 1—figure supplement 2
iEEG and LFP ripple characteristics with different detection thresholds.

(A) Distribution of iEEG ripple durations from all electrodes in all participants. (B) Distribution of iEEG ripple amplitudes from all electrodes in all participants. (C) Distribution of LFP ripple …

Figure 1—figure supplement 3
Multiple oscillations detection algorithm detected narrowband oscillations.

To complement our ripple detection method, we used the Multiple Oscillations Detection Algorithm, or MODAL, to detect narrowband oscillations (Watrous et al., 2018). This method identifies discrete …

Figure 1—figure supplement 4
MTL-ATL cross-correlograms with different detection thresholds.

To assess whether the ripples we detect in the cortex are associated with ripples observed in the medial temporal lobe (MTL), we measured the coupling of ripples between MTL and anterior temporal …

Figure 1—figure supplement 5
Interictal epileptiform discharge detection and overlap with ripples.

To confirm that the detected ripples are not an artifact of interictal epileptiform discharges (IEDs), we separately detected IEDs (see Materials and methods) and computed the overlap between …

Figure 1—figure supplement 6
High-frequency activity reflects discrete ripples.

(A) Surface-based regions of interest (ROIs) showing electrode coverage across 21 participants. (B) ROI plots of across-participant t-statistic for 70–200 Hz power and 80–120 Hz ripple rate for …

Figure 2 with 5 supplements
Ripple amplitudes reflect a spectrum of underlying local spiking activity.

(A) Locations of the microelectrode arrays (MEA) in six participants (top left). Location of the MEA with respect to four nearby iEEG channels in one participant (bottom left). Intraoperative photo …

Figure 2—source code 1

Matlab code of correlations between continuous spiking, LFP and iEEG.

https://cdn.elifesciences.org/articles/68401/elife-68401-fig2-code1-v2.zip
Figure 2—figure supplement 1
MEA position with respect to iEEG channels.

Position of MEA with respect to nearby iEEG channels in each participant.

Figure 2—figure supplement 2
Raw iEEG and LFP Trace.

Example raw iEEG in an anterior temporal lobe electrode and simultaneous LFP traces for one representative trial.

Figure 2—figure supplement 3
Spiking auto-correlograms within and outside ripples.

To confirm that ripples correspond to underlying bursts of spiking activity, we computed the population spiking auto-correlogram within and outside of each detected ripple event. (A) Population …

Figure 2—figure supplement 4
Ripple power and spike rate distributions.

We examiend whether the distribution of ripple band power in the iEEG and LFP signals, and the distribution of spiking activity, exhibit evidence of bimodality (see Materials and methods). (A) …

Figure 2—figure supplement 5
Ripples reflect underlying neuronal spiking.

(A) Pearson correlation between spike rate and continuous measures of the average LFP ripple amplitude over all micro-electrodes. Group level statistics are shown as mean ± SEM across six …

Figure 3 with 3 supplements
Macro-scale ripple amplitude reflects number and alignment of micro-scale ripples.

(A) Brief window around one iEEG ripple showing unfiltered iEEG signal (black), ripple band iEEG signal (blue) and ripple LFPs for one nearby iEEG channel and six microelectrode array (MEA) …

Figure 3—source code 1

Matlab code of pairwise phase consistency between LFP ripple signal and iEEG ripple amplitude.

https://cdn.elifesciences.org/articles/68401/elife-68401-fig3-code1-v2.zip
Figure 3—figure supplement 1
Macro-scale ripple amplitude reflects number and alignment of micro-scale ripples.

(A) Distribution of percentage of MEA electrodes containing LFP ripples that co-occur with iEEG ripples across all iEEG ripples in all participants. (B) Relation between percentage of MEA electrodes …

Figure 3—figure supplement 2
LFP-iEEG ripple cross-correlations for different detection thresholds.

(A) Example LFP-iEEG ripple cross-correlogram of true and shuffled events for one participant using a 2 SD amplitude and 10 ms duration ripple detect threshold (top) and a 3 SD amplitude and 25 ms …

Figure 3—figure supplement 3
LFP-iEEG ripple cross-correlations with respect to distance.

(A) Intraoperative photo of implanted MEA in the ATL (top) and after placement of an iEEG grid over the MEA (bottom). (B) Location of the MEA with respect to four nearby iEEG channels. (C) Subgroups …

Figure 4 with 2 supplements
Spiking activity is phase-locked to ripples and low frequencies.

(A) Brief window around one iEEG ripple and underlying LFP ripple and spiking activity. Dashed black lines indicate trough of iEEG ripple cycles compared to concurrent LFP ripple cycles and spiking. …

Figure 4—source code 1

Matlab code of pairwise phase consistency between spiking and LFP.

https://cdn.elifesciences.org/articles/68401/elife-68401-fig4-code1-v2.zip
Figure 4—figure supplement 1
Spiking activity is phase-locked to ripples and low frequencies.

(A) Spike-LFP phase-locking value (PLV) for each frequency shown as mean ± SEM across participants. PLV confirms that spiking activity is locked to low and high frequency activity across …

Figure 4—figure supplement 2
Spike-LFP PPC for different ripple detection thresholds.

Each bar shows the mean ± SEM spike-LFP PPC across participants.

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