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In vivo and in vitro electrochemical impedance spectroscopy analysis of acute and chronic intracranial electrodes

Cite this dataset

O'Sullivan, Kyle et al. (2024). In vivo and in vitro electrochemical impedance spectroscopy analysis of acute and chronic intracranial electrodes [Dataset]. Dryad. https://doi.org/10.5061/dryad.8931zcrvw

Abstract

Invasive intracranial electrodes are used in both clinical and research applications for recording and stimulation of brain tissue, providing essential data in acute and chronic contexts. The impedance characteristics of the electrode–tissue interface (ETI) evolve over time and can change dramatically relative to pre-implantation baseline. Understanding how ETI properties contribute to the recording and stimulation characteristics of an electrode can provide valuable insights for users who often do not have access to complex impedance characterizations of their devices. In contrast to the typical method of characterizing electrical impedance at a single frequency, we demonstrate a method for using electrochemical impedance spectroscopy (EIS) to investigate complex characteristics of the ETI of several commonly used acute and chronic electrodes. We also describe precise modeling strategies for verifying the accuracy of our instrumentation and understanding device–solution interactions, both in vivo and in vitro. Included with this publication is a dataset containing both in vitro and in vivo device characterizations, as well as some examples of modeling and error structure analysis results. These data can be used for more detailed interpretation of neural recordings performed on common electrode types, providing a more complete picture of their properties than is often available to users.

README: Electrochemical Impedance Spectroscopy (EIS) recordings of a series of implantable neural electrodes

This dataset contains both in-vitro and in-vivo EIS recordings of implantable electrodes designed for recording and stimulation of human and animal brain tissue. In-vitro data were recorded in up to four different electrolyte solutions and two different electrode configurations. Solutions included phosphate-buffered saline (PBS), artificial cerebrospinal fluid (ACSF) and salt solutions matching gray and white matter conductivities, in both two and three-electrode configurations. The counter electrode used in in-vivo measurements consisted of a titanium screw or titanium rod embedded in a chronically affixed skull cap, with its tip contacting brain tissue. Counter-electrodes used in vitro included a titanium screw similar to that used in vivo as well as platinum wire (7.5 cm length/0.5 mm diameter) and platinum foil (625 mm^2 surface area). When a 3-electrode measurement system was applied, the “reference” consisted of a silver-silver chloride (Ag/AgCl) electrode, as is typically employed in non-biological EIS applications. In vivo data were recorded from 2 chronically implanted adult male rhesus macaque monkeys, denoted as Animal 1 and Animal 2. In most cases, EIS measurements were performed three times to facilitate stochastic error structure modeling using the software and methods described here: https://ecsarxiv.org/kze9x/. This process can be used to assess signal to noise ratio (SNR) and perform other forms of modeling on the data. An example of the output from this process is included in the folder "Fitted model example", performed on a single channel of the segmented Heraeus lead from an in vitro recording.

Folder names within the dataset correspond to electrode models (name or model number), with the exception of "Bak Vs PalmSens", which contains data comparing the single-frequency Bak Electrode Impedance Tester to the Palmsens4 Potentiostat instrument, and "Fitted Model Example", which contains example modeling using the Measurement Model software (https://doi.org/10.1149/osf.io/kze9x).

File names in this dataset contain a description of the electrode model measured, the temperature at which measurements were conducted (for in vitro data), whether the measurement was conducted using a 2 or 3 electrode configuration, and the material/type of counter electrode used (or combined counter/reference for 2 electrode measurements). For example, the file "MDT_c1_37C_platWire_PBS.csv" contains data from the MDT SenSight electrode, contact one, recorded at 37 °C using a platinum wire counter-electrode in phosphate buffered saline solution. All 3-electrode measurements used a silver/silver chloride reference. When not otherwise noted, the fluid used in in-vitro measurements was PBS. Note that temperature measurements were accurate to within a tenth of a degree.

Data included here are encoded in both .csv and .pssession formats. The .csv files include columns for frequency, negative phase angle, DC current, complex impedance, real component of impedance, negative imaginary component of impedance, and charge. This file type should be readable by many types of software.

The included .pssession files are a proprietary format used by our PalmSens4 Potentiostat instrument's corresponding software, PSTrace (https://www.palmsens.com/software/ps-trace/). These files may be useful to others who use PalmSens instruments and software. A Python script used to convert from the .pssession file type to .csv format is also included, and is described below.

The python file, "pssession_parser.py"

converts *.pssession files to *.csv files.

This script works for python version 3.8+.

The script uses "Pandas" 1.1.1 for handling data.

In order to run this script, simply find the if \_name\_ == "main" statement,

change the datapath to either the *pssession file you are looking for or a directory of *pssession files you want to convert.

Then run the program to output the contents of the PalmSens .pssession file(s) as a .csv

Glossary:

* GM = Gray Matter

* WM = White Matter

* CSF = Cerebrospinal Fluid

* PBS = Phosphate Buffered Saline

* TR1/TR2/TR3=Trial one, Trial two, Trial three (as part of 3 repeated measurements)

* BF = Behnke Fried (Adtech BF) NP=NeuroPace

* 2-Electrode = Setups with 1 working electrode + 1 counter/reference electrode

* 3-Electrode = Setups with 1 working electrode, 1 counter electrode, 1 reference electrode

Methods

Electrochemical impedance spectroscopy- This technique involves measurement of an electrochemical interface by applying a sinusoidal voltage perturbation across a range of frequencies. For potentiostatic modulation, a single perturbation amplitude is maintained across the frequency spectrum, typically lower than amplitudes used in biological stimulation. The frequency range chosen for these measurements was 10 Hz-100 kHz, with an amplitude of 0.01 V. Data were sampled at 39 frequency intervals across this spectrum, or 9.5/dec. Using the complex impedance values obtained by our instrument, a fitted model was created to approximate the components of the biotic-abiotic interface.

Data collection- Data were primarily collected using a Palmsens4 Potentiostat instrument in Electrochemical Impedance Spectroscopy mode, both in vitro and in vivo in non-human primates (NHP). NHP subjects included two adult male rhesus macaque monkeys chronically implanted with both penetrating deep brain stimulation (DBS) electrodes and surface-contact electrocorticography (ECoG) electrodes placed epidurally. Measurements in vivo were performed only in 2-electrode mode, using a titanium screw or rod mounted to each animal’s skullcap as a return electrode. For in vitro measurements, a 2-electrode system was employed for direct comparison to typical in vivo data collection methods. A 3-electrode system including an Ag/AgCl reference electrode was also used in vitro to verify the reliability of the 2-electrode system. The Palmsens device was operated using battery power to isolate it from electrical line noise.

Sample fluids used in vitro included phosphate-buffered saline (PBS) at 1x concentration and artificial cerebrospinal fluid (aCSF). Sample fluid temperature was regulated to approximate biological conditions, specifically NHP internal body temperature of approximately 37° C. Temperature regulation was performed using a Gamry electrochemical flow-cell connected to a thermally regulated bath, with measured temperature verified to within plus or minus 0.1°C.

Working electrodes included a selection of commercially available intracranial electrodes, designed for both human and NHP applications. Electrodes used for in vivo measurements were chronically implanted, and connection to the Palmsens device was achieved via an external connector. The counter electrode used in vivo consisted of titanium screw for Animal 1 and a titanium rod for Animal 2, with the same approximate surface area. Counter electrodes used in vitro included a titanium screw similar to that used in vivo as well as platinum wire (7.5 cm length/0.5 mm diameter) and platinum foil (625 mm2). When a 3-electrode measurement system was applied, the “reference” consisted of a silver-silver chloride (Ag/AgCl) electrode, as is typically employed in non-biological EIS applications.

For comparison to standard methods of electrode impedance verification, measurements were also performed using a Bak Electrode Impedance Tester calibrated with a 1 kOhm resistor. In this setup, impedance was computed as a function of two contacts: a working electrode and a counter electrode.

Setup and solution preparation- Gray and white matter have measured conductivities of 0.33 and 0.142 S/m. The required salt concentration to mimic gray and white matter solutions was found by measuring the conductivity of dissolved salt at intervals of 0.5 g/L at 37°C +/- 0.1°C until the measured conductivity was greater than 0.33 S/m. Laboratory-grade salt (Thermo Fischer) was added between intervals, mixed using a vortex at 300 rpm until clear.  A line fit to these conductivity values was used to find salt concentrations that approximated the conductivity of gray and white matter. The aCSF was made using 12.6 mM NaCl, 3mM KCl, 26 mM NaHCO3, 1.4 mM NaH2PO4, 10mM Glucose, 2 mM CaCl2, and 2 mM MgSO4, osmolarity of 306 mOsm/L, and pH of 7.36.

For in vitro recordings, electrodes were suspended in solution with all contacts fully immersed in electrolyte and not touching glass side walls. EIS was measured using the Bak Electrode Impedance Tester and the PalmSens device. The PalmSens device delivered 10 Hz-10kHz, 0.1 nA-100 mAmps, 3 or 10 cycles each. The electrodes included in this solution comparison were AdTech Depth, AdTech Strip, AdTech Grid, Dixi Depth, Neuropace Depth, Neuropace Strip, and AdTech Behnke-Fried. To facilitate experimental determination of the stochastic error structure, trials were repeated 3x per electrode.

For in vivo recordings, the exposed distal end of the working electrode was accessed, and a titanium screw mounted in the NHP skullcap served as a combined counter/reference electrode. A Palmsens MUX8/R2 Multiplexer facilitated switching between channels of the working electrode, with three scans performed per channel to facilitate error regression.

Funding

National Institutes of Health, Award: NIH R01 NS111019