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Large-scale neural recordings with single neuron resolution using Neuropixels probes in human cortex

Paulk, Angelique C; Kfir, Yoav; Khanna, Arjun R; Mustroph, Martina L; Trautmann, Eric M; Soper, Dan J; Stavisky, Sergey D; Welkenhuysen, Marleen; Dutta, Barundeb; Shenoy, Krisha V; Hochberg, Leigh R; Richardson, R. Mark; Williams, Ziv M; Cash, Sydney S

Recent advances in multi-electrode array technology have made it possible to monitor large neuronal ensembles at cellular resolution in animal models. In humans, however, current approaches restrict recordings to few neurons per penetrating electrode or combine the signals of thousands of neurons in local field potential (LFP) recordings. Here, we describe a new probe variant and set of techniques which enable simultaneous recording from over 200 well-isolated cortical single units in human participants during intraoperative neurosurgical procedures using silicon Neuropixels probes. We characterized a diversity of extracellular waveforms with eight separable single unit classes, with differing firing rates, locations along the length of the electrode array, waveform spatial spread, and modulation by LFP events such as inter-ictal discharges and burst suppression. While some challenges remain in creating a turn-key recording system, high-density silicon arrays provide a path for studying human-specific cognitive processes and their dysfunction at unprecedented spatiotemporal resolution. 

We report and load only the three successful recordings from the cortex of temporal and frontal lobes in patients undergoing brain tissue resection to treat epilepsy (Pt. 03, N=1, under general anesthesia, lateral temporal lobe) or during the implantation of DBS leads to treat movement disorders (Pt. 01 and Pt. 02; N=2, one awake (Pt. 02) and one under general anesthesia (Pt. 01), dorsolateral prefrontal cortex) using Neuropixels probes. In our paper, we also reported unsuccessful recordings – and lessons learned -- from six cases performed while developing these approaches. Unsuccessful recordings were either due to electrode fracture (N=2, with the devices and pieces fully recovered) or excessive noise during the recordings (N=4). Two different types of arrays were tested. In the first two attempts, we used the original Neuropixels 1.0 probe but found it to be too fragile.  Instead, we developed a variant  featuring a thicker shank (Neuropixels 1.0-ST: thickness: 100µm, width: 70 µm, length: 10 mm). This version enabled considerably easier insertions and robust use during neurosurgical cases. This probe version, combined with an improved grounding and reference electrode configuration, enabled us to observe spiking activity from populations of isolatable single neurons in three participants (N=3, Pt. 01-03).

As we also observed movement artifact, we include both the raw data sampled during the recording in the operating room as well as teh interpolated data set (saved as a binary file) per participant for spike sorting. Further information is included in the ReadMe file: README_PaulkEtAlNeuropixels.txt

Data included from:
Participant Pt. 01, Neuropixels recording during a procedure for deep brain stimulation (DBS) surgery for treatment of a movement disorder, participant under generalized anesthesia; recording from right dorsolateral prefrontal cortex. 
Participant Pt. 02, Neuropixels recording during a procedure for deep brain stimulation (DBS) surgery for treatment of a movement disorder, participant awake and with monitored anesthesia care (MAC); recording from left dorsolateral prefrontal cortex.  
Participant Pt. 03, Neuropixels recording during a left anterior temporal lobectomy, under generalized anesthesia; recording from the left anterior temporal lobe. 

Further files are as such:

    A. raw recording Data, action potential (AP) band, binary file: Pt0X.imec0.ap.bin    
    B. meta data for the raw recording Data: Pt0X.imec0.ap.meta    
    C. raw recording Data, local field (LF) band, , binary file: Pt0X.imec0.lf.bin        
    D. meta data for the raw recording Data: Pt0X.imec0.lf.meta     
    F. recording Data realigned to adjust for movement, action potential (AP) band, binary file: Pt0X_aligned_0.bin

NOTE: For the Pt. 01 data set, the beginning included adjusting the ground and reference and inserting the electrode. For this reason, the aligned data for sorting (Pt01_aligned_0.bin) starts 330 sec into the recording. 

NOTE: For the Pt. 02 data set, the beginning included adjusting the ground and reference and inserting the electrode. For this reason, the aligned data for sorting (Pt02_aligned_0.bin) starts 220 sec into the recording. 

Funding provided by: ECOR*
Crossref Funder Registry ID:
Award Number:

Funding provided by: National Institutes of Health
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000002
Award Number: K24-NS088568

Funding provided by: Tiny Blue Dot Foundation
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100018260
Award Number:

Funding provided by: National Institute of Neurological Disorders and Stroke
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000065
Award Number: R01NS11662301

Funding provided by: National Institute on Deafness and Other Communication Disorders
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000055
Award Number: R01DC01403406

Funding provided by: Simons Foundation
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000893
Award Number: 543045

Funding provided by: Howard Hughes Medical Institute
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000011
Award Number: Stanford University

Funding provided by: A. P. Giannini Foundation
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100002112
Award Number:

Funding provided by: Wu Tsai Neurosciences Institute, Stanford University
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100014373
Award Number: Interdisciplinary Scholars Fellowship

Funding provided by: Burroughs Wellcome Fund
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000861
Award Number: Career Award at the Scientific Interface

Funding provided by: Brain and Behavior Research Foundation
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000874
Award Number:

Funding provided by: Grossman Institute*
Crossref Funder Registry ID:
Award Number:

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exportingCSVinfoExample.py
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extract_waveform_with_metrics.py
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Intarpolate_and_align_AP.m
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interpexample.png
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interpresult.png
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Load_CSV_from_blender.m
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main_pipeline.m
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Neuropixel_AP_preProcessing.m
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read_AP_from_bin.m
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read_LFP_from_bin.m
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README.md
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