Using fMRI to localize target regions for implanted brain-computer interfaces in locked-in syndrome

Sacha Leinders; Mariska J Vansteensel; Giovanni Piantoni; Mariana P Branco; Zac V Freudenburg; Tineke A Gebbink; Elmar G M Pels; Mathijs A H Raemaekers; Anouck Schippers; Erik J Aarnoutse; Nick F Ramsey

doi:10.1016/j.clinph.2023.08.003

Using fMRI to localize target regions for implanted brain-computer interfaces in locked-in syndrome

Sacha Leinders, Mariska J Vansteensel, Giovanni Piantoni, Mariana P Branco, Zac V Freudenburg, Tineke A Gebbink, Elmar G M Pels, Mathijs A H Raemaekers, Anouck Schippers, Erik J Aarnoutse, Nick F Ramsey^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

OBJECTIVE: Electrocorticography (ECoG)-based brain-computer interface (BCI) systems have the potential to improve quality of life of people with locked-in syndrome (LIS) by restoring their ability to communicate independently. Before implantation of such a system, it is important to localize ECoG electrode target regions. Here, we assessed the predictive value of functional magnetic resonance imaging (fMRI) for the localization of suitable target regions on the sensorimotor cortex for ECoG-based BCI in people with locked-in syndrome.

METHODS: Three people with locked-in syndrome were implanted with a chronic, fully implantable ECoG-BCI system. We compared pre-surgical fMRI activity with post-implantation ECoG activity from areas known to be active and inactive during attempted hand movement (sensorimotor hand region and dorsolateral prefrontal cortex, respectively).

RESULTS: Results showed a spatial match between fMRI activity and changes in ECoG low and high frequency band power (10 - 30 and 65 - 95 Hz, respectively) during attempted movement. Also, we found that fMRI can be used to select a sub-set of electrodes that show strong task-related signal changes that are therefore likely to generate adequate BCI control.

CONCLUSIONS: Our findings indicate that fMRI is a useful non-invasive tool for the pre-surgical workup of BCI implant candidates.

SIGNIFICANCE: If these results are confirmed in more BCI studies, fMRI might be used for more efficient surgical BCI procedures with focused cortical coverage and lower participant burden.

Original language	English
Pages (from-to)	1-15
Number of pages	15
Journal	Clinical Neurophysiology
Volume	155
Early online date	18 Aug 2023
DOIs	https://doi.org/10.1016/j.clinph.2023.08.003
Publication status	Published - Nov 2023

Keywords

Brain-computer interface
Electrocorticography
fMRI
Implant
Locked-in syndrome

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Leinders, S., Vansteensel, M. J., Piantoni, G., Branco, M. P., Freudenburg, Z. V., Gebbink, T. A., Pels, E. G. M., Raemaekers, M. A. H., Schippers, A., Aarnoutse, E. J., & Ramsey, N. F. (2023). Using fMRI to localize target regions for implanted brain-computer interfaces in locked-in syndrome. Clinical Neurophysiology, 155, 1-15. https://doi.org/10.1016/j.clinph.2023.08.003

@article{857bff6b4e13474e94e52142256480a7,

title = "Using fMRI to localize target regions for implanted brain-computer interfaces in locked-in syndrome",

abstract = "OBJECTIVE: Electrocorticography (ECoG)-based brain-computer interface (BCI) systems have the potential to improve quality of life of people with locked-in syndrome (LIS) by restoring their ability to communicate independently. Before implantation of such a system, it is important to localize ECoG electrode target regions. Here, we assessed the predictive value of functional magnetic resonance imaging (fMRI) for the localization of suitable target regions on the sensorimotor cortex for ECoG-based BCI in people with locked-in syndrome.METHODS: Three people with locked-in syndrome were implanted with a chronic, fully implantable ECoG-BCI system. We compared pre-surgical fMRI activity with post-implantation ECoG activity from areas known to be active and inactive during attempted hand movement (sensorimotor hand region and dorsolateral prefrontal cortex, respectively).RESULTS: Results showed a spatial match between fMRI activity and changes in ECoG low and high frequency band power (10 - 30 and 65 - 95 Hz, respectively) during attempted movement. Also, we found that fMRI can be used to select a sub-set of electrodes that show strong task-related signal changes that are therefore likely to generate adequate BCI control.CONCLUSIONS: Our findings indicate that fMRI is a useful non-invasive tool for the pre-surgical workup of BCI implant candidates.SIGNIFICANCE: If these results are confirmed in more BCI studies, fMRI might be used for more efficient surgical BCI procedures with focused cortical coverage and lower participant burden.",

keywords = "Brain-computer interface, Electrocorticography, fMRI, Implant, Locked-in syndrome",

author = "Sacha Leinders and Vansteensel, {Mariska J} and Giovanni Piantoni and Branco, {Mariana P} and Freudenburg, {Zac V} and Gebbink, {Tineke A} and Pels, {Elmar G M} and Raemaekers, {Mathijs A H} and Anouck Schippers and Aarnoutse, {Erik J} and Ramsey, {Nick F}",

note = "Funding Information: The authors thank Max van den Boom and Benny van der Vijgh for their work on research task software used in this study; Maxime Verwoert for her help with fMRI data acquisition and analysis; Vincent Kersten for maintaining our file server; UMCU ICU and radiology staff for their help during the fMRI session and in the week of implantation; UMCU clinical neurophysiology staff for their help with signal quality checks in the OR during the implantation and for their help with ECoG measurements in the days after implantation. The authors thank the participants and family and caregivers for their hard work, hospitality, and their courage. This work was funded by grants from the Dutch Organization for Scientific Research (NWO; Intense Project EU, work package 3), the Dutch Technology Foundation STW (STW 12803), and the National Institute for Deafness and other Communication Disorders (U01DC016686; U.S. NIH Grant/Contract). Medtronic provided implanted hardware as an in-kind contribution and provided technical support. NFR is co-founder and director at Braincarta, which specializes in off-the-shelf fMRI software for clinical assessment of brain anatomy and functioning. Braincarta software was not used for the analyses described in this manuscript. The authors report no other competing interests. Funding Information: This work was funded by grants from the Dutch Organization for Scientific Research (NWO; Intense Project EU, work package 3), the Dutch Technology Foundation STW (STW 12803), and the National Institute for Deafness and other Communication Disorders (U01DC016686; U.S. NIH Grant/Contract). Medtronic provided implanted hardware as an in-kind contribution and provided technical support. Publisher Copyright: {\textcopyright} 2023 International Federation of Clinical Neurophysiology",

year = "2023",

month = nov,

doi = "10.1016/j.clinph.2023.08.003",

language = "English",

volume = "155",

pages = "1--15",

journal = "Clinical Neurophysiology",

issn = "1388-2457",

publisher = "Elsevier Ireland Ltd",

}

TY - JOUR

T1 - Using fMRI to localize target regions for implanted brain-computer interfaces in locked-in syndrome

AU - Leinders, Sacha

AU - Vansteensel, Mariska J

AU - Piantoni, Giovanni

AU - Branco, Mariana P

AU - Freudenburg, Zac V

AU - Gebbink, Tineke A

AU - Pels, Elmar G M

AU - Raemaekers, Mathijs A H

AU - Schippers, Anouck

AU - Aarnoutse, Erik J

AU - Ramsey, Nick F

N1 - Funding Information: The authors thank Max van den Boom and Benny van der Vijgh for their work on research task software used in this study; Maxime Verwoert for her help with fMRI data acquisition and analysis; Vincent Kersten for maintaining our file server; UMCU ICU and radiology staff for their help during the fMRI session and in the week of implantation; UMCU clinical neurophysiology staff for their help with signal quality checks in the OR during the implantation and for their help with ECoG measurements in the days after implantation. The authors thank the participants and family and caregivers for their hard work, hospitality, and their courage. This work was funded by grants from the Dutch Organization for Scientific Research (NWO; Intense Project EU, work package 3), the Dutch Technology Foundation STW (STW 12803), and the National Institute for Deafness and other Communication Disorders (U01DC016686; U.S. NIH Grant/Contract). Medtronic provided implanted hardware as an in-kind contribution and provided technical support. NFR is co-founder and director at Braincarta, which specializes in off-the-shelf fMRI software for clinical assessment of brain anatomy and functioning. Braincarta software was not used for the analyses described in this manuscript. The authors report no other competing interests. Funding Information: This work was funded by grants from the Dutch Organization for Scientific Research (NWO; Intense Project EU, work package 3), the Dutch Technology Foundation STW (STW 12803), and the National Institute for Deafness and other Communication Disorders (U01DC016686; U.S. NIH Grant/Contract). Medtronic provided implanted hardware as an in-kind contribution and provided technical support. Publisher Copyright: © 2023 International Federation of Clinical Neurophysiology

PY - 2023/11

Y1 - 2023/11

N2 - OBJECTIVE: Electrocorticography (ECoG)-based brain-computer interface (BCI) systems have the potential to improve quality of life of people with locked-in syndrome (LIS) by restoring their ability to communicate independently. Before implantation of such a system, it is important to localize ECoG electrode target regions. Here, we assessed the predictive value of functional magnetic resonance imaging (fMRI) for the localization of suitable target regions on the sensorimotor cortex for ECoG-based BCI in people with locked-in syndrome.METHODS: Three people with locked-in syndrome were implanted with a chronic, fully implantable ECoG-BCI system. We compared pre-surgical fMRI activity with post-implantation ECoG activity from areas known to be active and inactive during attempted hand movement (sensorimotor hand region and dorsolateral prefrontal cortex, respectively).RESULTS: Results showed a spatial match between fMRI activity and changes in ECoG low and high frequency band power (10 - 30 and 65 - 95 Hz, respectively) during attempted movement. Also, we found that fMRI can be used to select a sub-set of electrodes that show strong task-related signal changes that are therefore likely to generate adequate BCI control.CONCLUSIONS: Our findings indicate that fMRI is a useful non-invasive tool for the pre-surgical workup of BCI implant candidates.SIGNIFICANCE: If these results are confirmed in more BCI studies, fMRI might be used for more efficient surgical BCI procedures with focused cortical coverage and lower participant burden.

AB - OBJECTIVE: Electrocorticography (ECoG)-based brain-computer interface (BCI) systems have the potential to improve quality of life of people with locked-in syndrome (LIS) by restoring their ability to communicate independently. Before implantation of such a system, it is important to localize ECoG electrode target regions. Here, we assessed the predictive value of functional magnetic resonance imaging (fMRI) for the localization of suitable target regions on the sensorimotor cortex for ECoG-based BCI in people with locked-in syndrome.METHODS: Three people with locked-in syndrome were implanted with a chronic, fully implantable ECoG-BCI system. We compared pre-surgical fMRI activity with post-implantation ECoG activity from areas known to be active and inactive during attempted hand movement (sensorimotor hand region and dorsolateral prefrontal cortex, respectively).RESULTS: Results showed a spatial match between fMRI activity and changes in ECoG low and high frequency band power (10 - 30 and 65 - 95 Hz, respectively) during attempted movement. Also, we found that fMRI can be used to select a sub-set of electrodes that show strong task-related signal changes that are therefore likely to generate adequate BCI control.CONCLUSIONS: Our findings indicate that fMRI is a useful non-invasive tool for the pre-surgical workup of BCI implant candidates.SIGNIFICANCE: If these results are confirmed in more BCI studies, fMRI might be used for more efficient surgical BCI procedures with focused cortical coverage and lower participant burden.

KW - Brain-computer interface

KW - Electrocorticography

KW - fMRI

KW - Implant

KW - Locked-in syndrome

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U2 - 10.1016/j.clinph.2023.08.003

DO - 10.1016/j.clinph.2023.08.003

M3 - Article

C2 - 37657190

SN - 1388-2457

VL - 155

SP - 1

EP - 15

JO - Clinical Neurophysiology

JF - Clinical Neurophysiology

ER -

Using fMRI to localize target regions for implanted brain-computer interfaces in locked-in syndrome

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Keywords

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