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
Affiliations
Julia P. Slopsema
Department of Biomedical Engineering, University of Minnesota
Antonietta Canna
Department of Radiology, Center for Magnetic Resonance Research, University of Minnesota
Michelle Uchenik
Department of Biomedical Engineering, University of Minnesota
Lauri J. Lehto
Department of Radiology, Center for Magnetic Resonance Research, University of Minnesota
Jordan Krieg
Department of Biomedical Engineering, University of Minnesota
Lucius Wilmerding
Department of Biomedical Engineering, University of Minnesota
Dee M. Koski
Department of Radiology, Center for Magnetic Resonance Research, University of Minnesota
Naoharu Kobayashi
Department of Radiology, Center for Magnetic Resonance Research, University of Minnesota
Joan Dao
Department of Biomedical Engineering, University of Minnesota
Madeline Blumenfeld
Department of Biomedical Engineering, University of Minnesota
Pavel Filip
Department of Radiology, Center for Magnetic Resonance Research, University of Minnesota; Department of Neurology, Charles University, First Faculty of Medicine and General University Hospital, Prague, Czech Republic
Hoon-Ki Min
Department of Radiology, Mayo Clinic
Silvia Mangia
Department of Radiology, Center for Magnetic Resonance Research, University of Minnesota; Joint senior authors
Matthew D. Johnson
Department of Biomedical Engineering, University of Minnesota; Institute for Translational Neuroscience, University of Minnesota; Joint senior authors
Shalom Michaeli
Department of Radiology, Center for Magnetic Resonance Research, University of Minnesota; Joint senior authors; Corresponding author.
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.
