A novel neural prosthesis providing long-term electrocorticography recording and cortical stimulation for epilepsy and brain-computer interface

Pantaleo RomanelliAB MEDICA S.p.a., Cerro Maggiore(MI), Milan;

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Marco PiangerelliComputer Science Division, School of Science and Technology, University of Camerino, Italy; and

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David RatelBiomedical Research Center, Polygone Scientifique Grenoble (CLINATEC Campus), University of Grenoble Alpes, Grenoble, France

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Christophe GaudeBiomedical Research Center, Polygone Scientifique Grenoble (CLINATEC Campus), University of Grenoble Alpes, Grenoble, France

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Thomas CostecaldeBiomedical Research Center, Polygone Scientifique Grenoble (CLINATEC Campus), University of Grenoble Alpes, Grenoble, France

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Cosimo PuttilliAB MEDICA S.p.a., Cerro Maggiore(MI), Milan;

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Mauro PicciafuocoAB MEDICA S.p.a., Cerro Maggiore(MI), Milan;

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Alim BenabidBiomedical Research Center, Polygone Scientifique Grenoble (CLINATEC Campus), University of Grenoble Alpes, Grenoble, France

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Napoleon TorresBiomedical Research Center, Polygone Scientifique Grenoble (CLINATEC Campus), University of Grenoble Alpes, Grenoble, France

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OBJECTIVE

Wireless technology is a novel tool for the transmission of cortical signals. Wireless electrocorticography (ECoG) aims to improve the safety and diagnostic gain of procedures requiring invasive localization of seizure foci and also to provide long-term recording of brain activity for brain-computer interfaces (BCIs). However, no wireless devices aimed at these clinical applications are currently available. The authors present the application of a fully implantable and externally rechargeable neural prosthesis providing wireless ECoG recording and direct cortical stimulation (DCS). Prolonged wireless ECoG monitoring was tested in nonhuman primates by using a custom-made device (the ECoG implantable wireless 16-electrode [ECOGIW-16E] device) containing a 16-contact subdural grid. This is a preliminary step toward large-scale, long-term wireless ECoG recording in humans.

METHODS

The authors implanted the ECOGIW-16E device over the left sensorimotor cortex of a nonhuman primate (Macaca fascicularis), recording ECoG signals over a time span of 6 months. Daily electrode impedances were measured, aiming to maintain the impedance values below a threshold of 100 KΩ. Brain mapping was obtained through wireless cortical stimulation at fixed intervals (1, 3, and 6 months). After 6 months, the device was removed. The authors analyzed cortical tissues by using conventional histological and immunohistological investigation to assess whether there was evidence of damage after the long-term implantation of the grid.

RESULTS

The implant was well tolerated; no neurological or behavioral consequences were reported in the monkey, which resumed his normal activities within a few hours of the procedure. The signal quality of wireless ECoG remained excellent over the 6-month observation period. Impedance values remained well below the threshold value; the average impedance per contact remains approximately 40 KΩ. Wireless cortical stimulation induced movements of the upper and lower limbs, and elicited fine movements of the digits as well. After the monkey was euthanized, the grid was found to be encapsulated by a newly formed dural sheet. The grid removal was performed easily, and no direct adhesions of the grid to the cortex were found. Conventional histological studies showed no cortical damage in the brain region covered by the grid, except for a single microscopic spot of cortical necrosis (not visible to the naked eye) in a region that had undergone repeated procedures of electrical stimulation. Immunohistological studies of the cortex underlying the grid showed a mild inflammatory process.

CONCLUSIONS

This preliminary experience in a nonhuman primate shows that a wireless neuroprosthesis, with related long-term ECoG recording (up to 6 months) and multiple DCSs, was tolerated without sequelae. The authors predict that epilepsy surgery could realize great benefit from this novel prosthesis, providing an extended time span for ECoG recording.

ABBREVIATIONS

BCI = brain-computer interface; DCS = direct cortical stimulation; ECoG = electrocorticography; ECOGIW-16E = ECoG implantable wireless 16-electrode; EEG = electroencephalography; GFAP = glial fibrillary acidic protein; Iba-1 = ionized calcium-binding adapter molecule–1; ISO = International Organization for Standardization; MICS = Medical Implant Communication Service; NT = neoformed tissue; SSEP = somatosensory evoked potential; Vim = vimentin.
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Illustration from Ferrareze Nunes et al. (pp 1304–1314). Copyright Juan C. Fernandez-Miranda. Published with permission.

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