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

Citation

Tong, Ai Phuong et al. (2021), Ripples reflect a spectrum of synchronous spiking activity in human anterior temporal lobe, Dryad, Dataset, https://doi.org/10.5061/dryad.5qfttdz6t

Abstract

Direct brain recordings have provided important insights into how high-frequency activity captured through intracranial EEG (iEEG) supports human memory retrieval. The extent to which such activity is comprised of transient fluctuations that reflect the dynamic coordination of underlying neurons, however, remains unclear. Here, we simultaneously record iEEG, local field potential (LFP), and single unit activity in the human temporal cortex. We demonstrate that fast oscillations within the previously identified 80–120 Hz ripple band contribute to broadband high-frequency activity in the human cortex. These ripple oscillations exhibit a spectrum of amplitudes and durations related to the amount of underlying neuronal spiking. Ripples in the macro-scale iEEG are related to the number and synchrony of ripples in the micro-scale LFP, which in turn are related to the synchrony of neuronal spiking. Our data suggest that neural activity in the human temporal lobe is organized into transient bouts of ripple oscillations that reflect underlying bursts of spiking activity.

Methods

Twenty-one participants with drug resistant epilepsy underwent a surgical procedure in which platinum recording contacts were implanted on the cortical surface as well as within the brain parenchyma. In each case, the clinical team determined the placement of the contacts to localize epileptogenic regions. In all the participants investigated here, the clinical region of investigation was the temporal lobes.

For research purposes, in six of these participants (4 female; 34.8 ± 4.7 years old) we placed one or two 96-channel microelectrode arrays (MEA; 4 × 4 mm, Cereplex I; Blackrock Microsystems, Inc, Salt Lake City, UT) in the anterior temporal lobe (ATL) in addition to the subdural contacts.

Intracranial EEG recordings

We collected intracranial EEG (iEEG) data from a total of 1660 subdural and depth recording contacts. Subdural contacts were arranged in both grid and strip configurations with an inter-contact spacing of 10 mm. We captured iEEG signals sampled at 1000 Hz. The recorded raw iEEG signals used for analyses were referenced to the system hardware reference, which was set by the recording amplifier (Nihon Kohden, Irvine CA) as the average of two intracranial electrode channels. We applied a local detrending procedure to remove slow fluctuations (≤ 2 Hz) from the time series of each electrode and a regression-based approach to remove line noise at 60 Hz and 120 Hz.

We quantified spectral power and phase in the iEEG signals by convolving the voltage time series with 200 linearly spaced complex valued Morlet wavelets between 2 and 200 Hz (wavelet number 6). We extracted data from all retrieval periods, beginning 4 s preceding vocalization to 1 s following vocalization and included a 1000 ms buffer on both sides of the clipped data. We squared and log-transformed the continuous-time wavelet transform to generate a continuous measure of instantaneous power for each frequency.

Microelectrode recordings

In six participants, we additionally captured spiking activity and micro-scale local field potentials (LFP) from the MEAs implanted in the anterior temporal lobe. Microelectrodes were arranged in a 10 × 10 grid with each electrode spaced 400 μm apart and extending 1.5 mm into the cortical surface (1.0 mm for one participant). Post-operative paraffin blocks of the resected tissue demonstrated that the electrodes extended approximately halfway into the 3-mm-thick gray matter. We digitally recorded microelectrode signals at 30 kHz using the Cereplex I and a Cerebus acquisition system (Blackrock Microsystems), with 16-bit precision and a range of ± 8 mV.

To extract unit spiking activity, we re-referenced each electrode’s signal offline by subtracting the mean signal of all the electrodes in the MEA, and then used a second order Butterworth filter to bandpass the signal between 0.3 and 3 kHz. Using a spike-sorting software package (Plexon Offline Sorter, Dallas, TX, USA), we identified spike waveforms by manually setting a negative or positive voltage threshold depending on the direction of putative action potentials. The voltage threshold was set to include noise signals used in calculating unit isolation quality (see below). Waveforms (duration, 1.067 ms; 32 samples per waveform) that crossed the voltage threshold were stored for spike sorting. Spike clusters were manually identified by viewing the first two principal components, and the difference in peak-to-trough voltage (voltage versus time) of the waveforms. We manually drew a boundary around clusters of waveforms that were differentiable from noise throughout the experimental session. In this manner, we identified a total of 989 putative single units across all sessions (average of 72 ± 21 units per participant). The average spike rate across all units was 2.82 ± .01 Hz. In addition to the spiking data, we also used a 500 Hz low pass filter to extract the LFP signals from each microelectrode, down-sampled to 1000 Hz, and then performed a similar line noise removal and channel selection procedure to that used for the iEEG channels to exclude artifacts related to epileptiform activity or other system level noise. Across the six participants, after pre-processing we retained recordings from 78 ± 27 MEA electrodes for further analysis.

Usage Notes

There are accompanying data files loaded by four Matlab scripts to show representative examples for four main figures.

There are four data files for Figure 1, includes iEEG signals from medial temporal lobe in one representative participant.

There is one data file for Figure 2, includes iEEG signals from temporal lobe and simultaneous LFP and spiking data in one representative participant.

There are two data files for Figure 3, includes simultaneous iEEG signals and simultaneous spike phase locking data for one representative participant.

There is one data file for Figure 4, includes spiking-LFP phase locking data for one representative participant.

Funding

National Institutes of Health, Award: Intramural Research Program

National Institutes of Health, Award: F31 NS113400