Orientation-selective and directional deep brain stimulation in swine assessed by functional MRI at 3T

Julia P. Slopsema; Antonietta Canna; Michelle Uchenik; Lauri J. Lehto; Jordan Krieg; Lucius Wilmerding; Dee M. Koski; Naoharu Kobayashi; Joan Dao; Madeline Blumenfeld; Pavel Filip; Hoon Ki Min; Silvia Mangia; Matthew D. Johnson; Shalom Michaeli

doi:10.1016/j.neuroimage.2020.117357

Orientation-selective and directional deep brain stimulation in swine assessed by functional MRI at 3T

Julia P. Slopsema, Antonietta Canna, Michelle Uchenik, Lauri J. Lehto, Jordan Krieg, Lucius Wilmerding, Dee M. Koski, Naoharu Kobayashi, Joan Dao, Madeline Blumenfeld, Pavel Filip, Hoon Ki Min, Silvia Mangia, Matthew D. Johnson, Shalom Michaeli

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

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Abstract

Functional MRI (fMRI) has become an important tool for probing network-level effects of deep brain stimulation (DBS). Previous DBS-fMRI studies have shown that electrical stimulation of the ventrolateral (VL) thalamus can modulate sensorimotor cortices in a frequency and amplitude dependent manner. Here, we investigated, using a swine animal model, how the direction and orientation of the electric field, induced by VL-thalamus DBS, affects activity in the sensorimotor cortex. Adult swine underwent implantation of a novel 16-electrode (4 rows x 4 columns) directional DBS lead in the VL thalamus. A within-subject design was used to compare fMRI responses for (1) directional stimulation consisting of monopolar stimulation in four radial directions around the DBS lead, and (2) orientation-selective stimulation where an electric field dipole was rotated 0°-360° around a quadrangle of electrodes. Functional responses were quantified in the premotor, primary motor, and somatosensory cortices. High frequency electrical stimulation through leads implanted in the VL thalamus induced directional tuning in cortical response patterns to varying degrees depending on DBS lead position. Orientation-selective stimulation showed maximal functional response when the electric field was oriented approximately parallel to the DBS lead, which is consistent with known axonal orientations of the cortico-thalamocortical pathway. These results demonstrate that directional and orientation-selective stimulation paradigms in the VL thalamus can tune network-level modulation patterns in the sensorimotor cortex, which may have translational utility in improving functional outcomes of DBS therapy.

Original language	English (US)
Article number	117357
Journal	NeuroImage
Volume	224
DOIs	https://doi.org/10.1016/j.neuroimage.2020.117357
State	Published - Jan 1 2021

Bibliographical note

Funding Information:
This work was supported by the National Institutes of Health ( R01-NS081118 , R01-NS094206 , P50-NS098573 , U01-NS103569 ), NSF-GRFP (00039202, JPS), and the EU H2020 Marie Skłodowska RISE project (#691110, MICROBRADAM). We thank the Center for Magnetic Resonance Research (NIH core grants: P41-EB015894, P30-NS076408, U54-MH091657) and University of Minnesota Foundation for help with the MRI imaging used in this study (Dee Koski, Erik Solheid). We thank Heraeus Medical Components for the DBS lead (Robert Cass, Mark Hjelle, Mitch Lark, Paul Noffke, David Ohmann), NRTL lab members (Lauren Madden, Annie Brinda, Mojgan Goftari), and the Mayo Clinic Neuroengineering Group for guidance and fabrication of the stereotactic frame and targeting software (Dr. Kendall Lee, Steven Goerss, Dr. Joshua Jacobs).

Publisher Copyright:
© 2020

Keywords

Directional DBS
Functional magnetic resonance imaging
High frequency stimulation
Motor cortex
Orientation selective DBS
Somatosensory cortex
Thalamus

Center for Magnetic Resonance Research (CMRR) tags

NM
P41

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10.1016/j.neuroimage.2020.117357

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Slopsema, J. P., Canna, A., Uchenik, M., Lehto, L. J., Krieg, J., Wilmerding, L., Koski, D. M., Kobayashi, N., Dao, J., Blumenfeld, M., Filip, P., Min, H. K., Mangia, S., Johnson, M. D., & Michaeli, S. (2021). Orientation-selective and directional deep brain stimulation in swine assessed by functional MRI at 3T. NeuroImage, 224, Article 117357. https://doi.org/10.1016/j.neuroimage.2020.117357

@article{7b8ed517b8bb4923882a602ec9efd50e,

title = "Orientation-selective and directional deep brain stimulation in swine assessed by functional MRI at 3T",

abstract = "Functional MRI (fMRI) has become an important tool for probing network-level effects of deep brain stimulation (DBS). Previous DBS-fMRI studies have shown that electrical stimulation of the ventrolateral (VL) thalamus can modulate sensorimotor cortices in a frequency and amplitude dependent manner. Here, we investigated, using a swine animal model, how the direction and orientation of the electric field, induced by VL-thalamus DBS, affects activity in the sensorimotor cortex. Adult swine underwent implantation of a novel 16-electrode (4 rows x 4 columns) directional DBS lead in the VL thalamus. A within-subject design was used to compare fMRI responses for (1) directional stimulation consisting of monopolar stimulation in four radial directions around the DBS lead, and (2) orientation-selective stimulation where an electric field dipole was rotated 0°-360° around a quadrangle of electrodes. Functional responses were quantified in the premotor, primary motor, and somatosensory cortices. High frequency electrical stimulation through leads implanted in the VL thalamus induced directional tuning in cortical response patterns to varying degrees depending on DBS lead position. Orientation-selective stimulation showed maximal functional response when the electric field was oriented approximately parallel to the DBS lead, which is consistent with known axonal orientations of the cortico-thalamocortical pathway. These results demonstrate that directional and orientation-selective stimulation paradigms in the VL thalamus can tune network-level modulation patterns in the sensorimotor cortex, which may have translational utility in improving functional outcomes of DBS therapy.",

keywords = "Directional DBS, Functional magnetic resonance imaging, High frequency stimulation, Motor cortex, Orientation selective DBS, Somatosensory cortex, Thalamus",

author = "Slopsema, {Julia P.} and Antonietta Canna and Michelle Uchenik and Lehto, {Lauri J.} and Jordan Krieg and Lucius Wilmerding and Koski, {Dee M.} and Naoharu Kobayashi and Joan Dao and Madeline Blumenfeld and Pavel Filip and Min, {Hoon Ki} and Silvia Mangia and Johnson, {Matthew D.} and Shalom Michaeli",

note = "Funding Information: This work was supported by the National Institutes of Health ( R01-NS081118 , R01-NS094206 , P50-NS098573 , U01-NS103569 ), NSF-GRFP (00039202, JPS), and the EU H2020 Marie Sk{\l}odowska RISE project (#691110, MICROBRADAM). We thank the Center for Magnetic Resonance Research (NIH core grants: P41-EB015894, P30-NS076408, U54-MH091657) and University of Minnesota Foundation for help with the MRI imaging used in this study (Dee Koski, Erik Solheid). We thank Heraeus Medical Components for the DBS lead (Robert Cass, Mark Hjelle, Mitch Lark, Paul Noffke, David Ohmann), NRTL lab members (Lauren Madden, Annie Brinda, Mojgan Goftari), and the Mayo Clinic Neuroengineering Group for guidance and fabrication of the stereotactic frame and targeting software (Dr. Kendall Lee, Steven Goerss, Dr. Joshua Jacobs). Publisher Copyright: {\textcopyright} 2020",

year = "2021",

month = jan,

day = "1",

doi = "10.1016/j.neuroimage.2020.117357",

language = "English (US)",

volume = "224",

journal = "NeuroImage",

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TY - JOUR

T1 - Orientation-selective and directional deep brain stimulation in swine assessed by functional MRI at 3T

AU - Slopsema, Julia P.

AU - Canna, Antonietta

AU - Uchenik, Michelle

AU - Lehto, Lauri J.

AU - Krieg, Jordan

AU - Wilmerding, Lucius

AU - Koski, Dee M.

AU - Kobayashi, Naoharu

AU - Dao, Joan

AU - Blumenfeld, Madeline

AU - Filip, Pavel

AU - Min, Hoon Ki

AU - Mangia, Silvia

AU - Johnson, Matthew D.

AU - Michaeli, Shalom

N1 - Funding Information: This work was supported by the National Institutes of Health ( R01-NS081118 , R01-NS094206 , P50-NS098573 , U01-NS103569 ), NSF-GRFP (00039202, JPS), and the EU H2020 Marie Skłodowska RISE project (#691110, MICROBRADAM). We thank the Center for Magnetic Resonance Research (NIH core grants: P41-EB015894, P30-NS076408, U54-MH091657) and University of Minnesota Foundation for help with the MRI imaging used in this study (Dee Koski, Erik Solheid). We thank Heraeus Medical Components for the DBS lead (Robert Cass, Mark Hjelle, Mitch Lark, Paul Noffke, David Ohmann), NRTL lab members (Lauren Madden, Annie Brinda, Mojgan Goftari), and the Mayo Clinic Neuroengineering Group for guidance and fabrication of the stereotactic frame and targeting software (Dr. Kendall Lee, Steven Goerss, Dr. Joshua Jacobs). Publisher Copyright: © 2020

PY - 2021/1/1

Y1 - 2021/1/1

N2 - Functional MRI (fMRI) has become an important tool for probing network-level effects of deep brain stimulation (DBS). Previous DBS-fMRI studies have shown that electrical stimulation of the ventrolateral (VL) thalamus can modulate sensorimotor cortices in a frequency and amplitude dependent manner. Here, we investigated, using a swine animal model, how the direction and orientation of the electric field, induced by VL-thalamus DBS, affects activity in the sensorimotor cortex. Adult swine underwent implantation of a novel 16-electrode (4 rows x 4 columns) directional DBS lead in the VL thalamus. A within-subject design was used to compare fMRI responses for (1) directional stimulation consisting of monopolar stimulation in four radial directions around the DBS lead, and (2) orientation-selective stimulation where an electric field dipole was rotated 0°-360° around a quadrangle of electrodes. Functional responses were quantified in the premotor, primary motor, and somatosensory cortices. High frequency electrical stimulation through leads implanted in the VL thalamus induced directional tuning in cortical response patterns to varying degrees depending on DBS lead position. Orientation-selective stimulation showed maximal functional response when the electric field was oriented approximately parallel to the DBS lead, which is consistent with known axonal orientations of the cortico-thalamocortical pathway. These results demonstrate that directional and orientation-selective stimulation paradigms in the VL thalamus can tune network-level modulation patterns in the sensorimotor cortex, which may have translational utility in improving functional outcomes of DBS therapy.

AB - Functional MRI (fMRI) has become an important tool for probing network-level effects of deep brain stimulation (DBS). Previous DBS-fMRI studies have shown that electrical stimulation of the ventrolateral (VL) thalamus can modulate sensorimotor cortices in a frequency and amplitude dependent manner. Here, we investigated, using a swine animal model, how the direction and orientation of the electric field, induced by VL-thalamus DBS, affects activity in the sensorimotor cortex. Adult swine underwent implantation of a novel 16-electrode (4 rows x 4 columns) directional DBS lead in the VL thalamus. A within-subject design was used to compare fMRI responses for (1) directional stimulation consisting of monopolar stimulation in four radial directions around the DBS lead, and (2) orientation-selective stimulation where an electric field dipole was rotated 0°-360° around a quadrangle of electrodes. Functional responses were quantified in the premotor, primary motor, and somatosensory cortices. High frequency electrical stimulation through leads implanted in the VL thalamus induced directional tuning in cortical response patterns to varying degrees depending on DBS lead position. Orientation-selective stimulation showed maximal functional response when the electric field was oriented approximately parallel to the DBS lead, which is consistent with known axonal orientations of the cortico-thalamocortical pathway. These results demonstrate that directional and orientation-selective stimulation paradigms in the VL thalamus can tune network-level modulation patterns in the sensorimotor cortex, which may have translational utility in improving functional outcomes of DBS therapy.

KW - Directional DBS

KW - Functional magnetic resonance imaging

KW - High frequency stimulation

KW - Motor cortex

KW - Orientation selective DBS

KW - Somatosensory cortex

KW - Thalamus

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DO - 10.1016/j.neuroimage.2020.117357

M3 - Article

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SN - 1053-8119

VL - 224

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JF - NeuroImage

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ER -

Orientation-selective and directional deep brain stimulation in swine assessed by functional MRI at 3T

Abstract

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Keywords

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