Intraoperative fiber optic guidance during chronic electrode implantation in deep brain stimulation neurosurgery: proof of concept in primates

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OBJECTIVE

The clinical outcome of deep brain stimulation (DBS) surgery relies heavily on the implantation accuracy of a chronic stimulating electrode into a small target brain region. Most techniques that have been proposed to precisely target these deep brain regions were designed to map intracerebral electrode trajectory prior to chronic electrode placement, sometimes leading to positioning error of the final electrode. This study was designed to create a new intraoperative guidance tool for DBS neurosurgery that can improve target detection during the final implantation of the chronic electrode.

METHODS

Taking advantage of diffuse reflectance spectroscopy, the authors developed a new surgical tool that senses proximal brain tissue through the tip of the chronic electrode by means of a novel stylet, which provides rigidity to DBS leads and houses fiber optics.

RESULTS

As a proof of concept, the authors demonstrated the ability of their noninvasive optical guidance technique to precisely locate the border of the subthalamic nucleus during the implantation of commercially available DBS electrodes in anesthetized parkinsonian monkeys. Innovative optical recordings combined to standard microelectrode mapping and detailed postmortem brain examination allowed the authors to confirm the precision of optical target detection. They also show the optical technique’s ability to detect, in real time, upcoming blood vessels, reducing the risk of hemorrhage during the chronic lead implantation.

CONCLUSIONS

The authors present a new optical guidance technique that can detect target brain regions during DBS surgery from within the implanted electrode using a proof of concept in nonhuman primates. The technique discriminates tissue in real time, contributes no additional invasiveness to the procedure by being housed within the electrode, and can provide complementary information to microelectrode mapping during the implantation of the chronic electrode. The technique may also be a powerful tool for providing direct anatomical information in the case of direct implantations wherein microelectrode mapping is not performed.

ABBREVIATIONS DBS = deep brain stimulation; DRS = diffuse reflectance spectroscopy; GPe = globus pallidus pars externa; GPi = globus pallidus pars interna; MER = microelectrode recording; NHP = nonhuman primate; NIR = near infrared; PCA = principal component analysis; STN = subthalamic nucleus.

Article Information

Correspondence Daniel C. Côté: Université Laval, Quebec City, QC, Canada. dccote@cervo.ulaval.ca.

INCLUDE WHEN CITING Published online May 31, 2019; DOI: 10.3171/2019.1.JNS182600.

Disclosures Prof. Côté: ownership in Bliq Photonics.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Setup and probes. A: Back end of the optical fiber–containing stylet and Medtronic 3389 DBS lead. B: Front end of optical fiber containing the stylet, Medtronic 3389 DBS lead, and in-house cannula. C: Medtronic 3389 DBS lead with optical fibers inserted, showing light transmission through the semitransparent tip. D: The tip of the optical microelectrode probe is used to measure neuronal activity and optical information simultaneously. Figure is available in color online only.

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    Data analysis A: Example spectra measure from different sections of fresh NHP tissue. B: Example component scores from PCA analysis over an entire trajectory during a DBS electrode implantation in an NHP. C: Example of the intensity at 800 nm over an entire trajectory during a DBS electrode implantation in an NHP where the probe passed only through the internal capsule until the STN target structure. D: Example of discrimination over the same trajectory using the normalized intensity at 800 nm and the linear regression–calculated contributions of each of the 4 preloaded PCA components describing a single spectral acquisition. The 5 variables are thresholded at their median, and the algorithm chooses if a tissue is white, gray, or mixed matter or a blood vessel based on the thresholded binary pattern. The color coding is designed for easy understanding of the sequence of brain structures passed along the trajectory of implantation. a.u. = arbitrary unit. Figure is available in color online only.

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    Ex vivo blood vessel detection in NHP tissue. Left: Brain and blood vessel slice. The colored bar shows the automated discrimination of the blood vessel and the small gray matter area. The data began to be acquired at position 0 mm denoted by the square end of the arrow and ended at 4 mm denoted by the arrow tip. Right: Single wavelength reflectance values over the length of the scan showing that the wavelengths are not able to discriminate between the blood vessel and gray matter region, unlike the DRS algorithm. The red rectangle overlay signifies where the blood vessel was located. Figure is available in color online only.

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    In vivo dual MER and optical probe implantation for comparing concurrent optical and electrical measurements in NHP DBS implantation. A: NIR intensity over the trajectory through the brain is shown, starting near the cortex/white matter boundary. The numbers within the graph refer to locations of concurrent neuronal recordings. Red sections signify algorithm-detected white matter. The discrimination plot is superimposed over the area where the probe was sent down during surgery with the region numbers referring to the following: 1, cortical white matter; 2, caudate nucleus; 3; medial aspect of the internal capsule/stria terminalis; 4 and 5, thalamus; 6, zona incerta; and T (for target), STN. B: Electrical recordings at various stages throughout the trajectory are shown. STN activity begins at 22.5 mm, again denoted as region T for target. C: Postmortem slice of brain fixed with the implanted probe to show true location. Figure is available in color online only.

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    Ex vivo stereotactic dual-angle DBS lead implantation in an NHP with fiber optic stylet, on target. The arrow indicates the electrode. A: Lead implant location in the left hemisphere of the NHP’s brain. Inset: Sagittal view showing the dual-angle trajectory. B: Postmortem brain slice where implantation occurred. The calculated position on an atlas image according to the radiography measurements made during the implantation (inset). A discrimination plot is superimposed over the area where the probe was sent down during the surgery with the region numbers referring to the following: 1, cortex; 2, cortical white matter; 3, GPe; 4, internal capsule; and 5, STN. The algorithm labeled the substantia nigra (SN) as mixed matter, but with future iterations it will include the substantia nigra as a unique tissue subcategory since it does have a unique spectral signature caused by the strong visible chromophore melanin. The GPe is detected as a mix of gray and mixed matter, which is reasonable depending on the location of the probe in the structure (i.e., edge vs central). The GPe is outlined manually since the contrast is not optimal. C: NIR intensity plot over the trajectory starting at the cortex/white matter boundary. Region numbers located in the position along the trajectory correspond to their respective brain regions according to the brain slice. Red sections signify algorithm-detected white matter. Inset in panel B modified with permission from Szabo J, Cowan WM: A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis). J Comp Neurol 222:265–300, 1984. Copyright Alan R. Liss, Inc. (now owned by John Wiley and Sons). Figure is available in color online only.

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    In vivo stereotactic single-angle DBS lead implantation in an NHP, off target. The arrow indicates the electrode. A: Radiograph showing the lead implant location in the left hemisphere of the NHP’s brain. B: Postmortem brain slice where implantation occurred. The calculated position designated by the cross-hairs on an atlas image according to the radiography measurements made during the implantation (inset). The discrimination plot is superimposed over the area where the probe was sent down during the surgery with the region numbers referring to the following: 1, white matter; 2, caudate nucleus; 3, white matter; and 4, thalamus. C: NIR intensity plot over the trajectory starting at the cortex/white matter boundary. Region numbers located in the position along the trajectory correspond to their respective brain regions according to the brain slice. Red sections signify algorithm-detected white matter. Inset in panel B modified with permission from Szabo J, Cowan WM: A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis). J Comp Neurol 222:265–300, 1984. Copyright Alan R. Liss, Inc. (now owned by John Wiley and Sons). Figure is available in color online only.

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