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

. 2021 Jan 01 ; 224 () : 117357. [epub] 20200909

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid32916285

Grantová podpora
P41 EB027061 NIBIB NIH HHS - United States
P50 NS098573 NINDS NIH HHS - United States
P41 EB015894 NIBIB NIH HHS - United States
R01 NS094206 NINDS NIH HHS - United States
P30 NS076408 NINDS NIH HHS - United States
U01 NS103569 NINDS NIH HHS - United States
U54 MH091657 NIMH NIH HHS - United States
R25 NS118756 NINDS NIH HHS - United States
R01 NS081118 NINDS NIH HHS - United States

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.

Zobrazit více v PubMed

Anderson DN, Duffley G, Vorwerk J, Dorval AD, Butson CR, 2019. Anodic stimulation misunderstood: preferential activation of fiber orientations with anodic waveforms in deep brain stimulation. J Neural Eng 16 (1), 016026. doi: 10.1088/1741-2552/aae590. PubMed DOI PMC

Asanuma C, Thach T, Jones EG, 1983. Distribution of cerebellar terminations in the ventral lateral thalamic region of the monkey. Brain ResRev 5, 237–265. PubMed

Barbe MT, Maarouf M, Alesch F, Timmermann L, 2014. Multiple source current steering–a novel deep brain stimulation concept for customized programming in a Parkinson’s disease patient. Parkinsonism Relat. Disord 20 (4), 471–473. doi: 10.1016/j.parkreldis.2013.07.021. PubMed DOI

Benabid AL, Pollak P, Hoffmann D, et al., 1991. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. The Lancet 337 (8738), 403–406. doi: 10.1016/0140-6736(91)91175-T. PubMed DOI

Bergin CJ, Pauly JM, Macovski A, 1991. Lung Parenchyma: projection Reconstruction MR Imaging. Radiology 777–781 Published online. PubMed

Butson CR, McIntyre CC, 2008. Current steering to control the volume of tissue activated during deep brain stimulation. Brain Stimul 1 (1), 7–15. doi: 10.1016/j.brs.2007.08.004. PubMed DOI PMC

Carmichael DW, Pinto S, Limousin-Dowsey P, et al., 2007. Functional MRI with active, fully implanted, deep brain stimulation systems: safety and experimental confounds. Neuroimage 37 (2), 508–517. doi: 10.1016/j.neuroimage.2007.04.058. PubMed DOI

Ceballos-Baumann AO, Boecker H, Fogel W, et al., 2001. Thalamic stimulation for essential tremor activates motor and deactivates vestibular cortex. Neurology 56 (10), 1347–1354. PubMed

Chaturvedi A, Luján JL, McIntyre CC, 2013. Artificial neural network based characterization of the volume of tissue activated during deep brain stimulation. J Neural Eng 10 (5), 056023. doi: 10.1088/1741-2560/10/5/056023. PubMed DOI PMC

Connolly AT, Vetter RJ, Hetke JF, et al., 2016. A Novel Lead Design for Modulation and Sensing of Deep Brain Structures. IEEE Transactions on Biomedical Engineering 63 (1), 148–157. doi: 10.1109/TBME.2015.2492921. PubMed DOI PMC

Contarino MF, Bour LJ, Verhagen R, et al., 2014. Directional steering: a novel approach to deep brain stimulation. Neurology 83 (13), 1163–1169. doi: 10.1212/WNL.0000000000000823. PubMed DOI

Dembek TA, Reker P, Visser-Vandewalle V, et al., 2017. Directional DBS increases side-effect thresholds-A prospective, double-blind trial: directional Dbs Increases Side-Effect Thresholds. Movement Disorders 32 (10), 1380–1388. doi: 10.1002/mds.27093. PubMed DOI

Edwards CA, Rusheen AE, Oh Y, et al., 2018. A novel re-attachable stereotactic frame for MRI-guided neuronavigation and its validation in a large animal and human cadaver model. J Neural Eng 15 (6), 066003. doi: 10.1088/1741-2552/aadb49. PubMed DOI PMC

Fang P−C, Stepniewska I, Kaas JH, 2006. The thalamic connections of motor, premotor, and prefrontal areas of cortex in a prosimian primate (Otolemur garnetti). Neuroscience 143 (4), 987–1020. doi: 10.1016/j.neuroscience.2006.08.053. PubMed DOI PMC

Fedorov A, Beichel R, Kalpathy-Cramer J, et al., 2012. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging 30 (9), 1323–1341. doi: 10.1016/j.mri.2012.05.001. PubMed DOI PMC

Félix B, Léger M−E, Albe-Fessard D, et al., 1999. Stereotaxic atlas of the pig brain. Brain Res. Bull 49 (1), 1–137. PubMed

Fytagoridis A, Sjöberg R, Åström M, Fredricks A, 2013. Effects of deep brain stimulation in the caudal Zona incerta on verbal fluency. S Karger 91 (1), 24–29. doi: 10.1159/000342497. PubMed DOI

Gibson WS, Jo HJ, Testini P, et al., 2016. Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor. Brain 139 (8), 2198–2210. doi: 10.1093/brain/aww145. PubMed DOI PMC

Gorny KR, Presti MF, Goerss SJ, et al., 2013. Measurements of RF heating during 3.0-T MRI of a pig implanted with deep brain stimulator. Magn Reson Imaging 31 (5), 783–788. doi: 10.1016/j.mri.2012.11.005. PubMed DOI PMC

Guillery RW, 1995. Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. Journal of Anantomy 187, 583–592. PubMed PMC

Hamel W, Herzog J, Kopper F, et al., 2007. Deep brain stimulation in the subthalamic area is more effective than nucleus ventralis intermedius stimulation for bilateral intention tremor. Acta Neurochir (Wien) 149 (8), 749–758. doi: 10.1007/s00701-007-1230-1. PubMed DOI

Hartmann CJ, Hirschmann J, Vesper J, Wojtecki L, Butz M, Schnitzler A, 2018. Distinct cortical responses evoked by electrical stimulation of the thalamic ventral intermediate nucleus and of the subthalamic nucleus. NeuroImage: Clinical 20, 1246–1254. doi: 10.1016/j.nicl.2018.11.001. PubMed DOI PMC

Haslinger B, Boecker H, Büchel C, et al., 2003. Differential modulation of subcortical target and cortex during deep brain stimulation. Neuroimage 18 (2), 517–524. doi: 10.1016/S1053-8119(02)00043-5. PubMed DOI

Hofman MA.., 1985. Size and Shape of the Cerebral Cortex in Mammals. I. The Cortical Surface. Brain, Behavior & Evolution 27, 28–34. PubMed

Hua SE, Lenz FA, Zirh TA, Reich SG, Dougherty PM, 1998. Thalamic neuronal activity correlated with essential tremor. Journal of Neurology, Neurosurgery & Psychiatry 64 (2), 273–276. PubMed PMC

Hubble J, Busenbark K, Wilkinson S, Penn R, Lyons K, Koller W, 1996. Deep brain stimulation for essential tremor. Neurology 46, 1150–1153. PubMed

Ilinsky I, Kultas-Ilinsky K, 1987. Sagittal cytoarchitectonic maps of the macaca mulatta thalamus with a revised nomenclature of the motor-related nuclei validated by observations on their connectivity. JCompNeurol 262, 331–364. PubMed

Ilinsky IA, Kultas-Ilinsky K, 2002. Motor thalamic circuits in primates with emphasis on the area targeted in treatment of movement disorders. Movement Disorders 17 (S3), S9–S14. doi: 10.1002/mds.10137. PubMed DOI

Kakei S, Na J, Shinoda Y, 2001. Thalamic terminal morphology and distribution of single corticothalamic axons originating from layers 5 and 6 of the cat motor cortex. J. Comp. Neurol 437 (2), 170–185. doi: 10.1002/cne.1277. PubMed DOI

Keane M, Deyo S, Abosch A, Bajwa JA, Johnson MD, 2012. Improved spatial targeting with directionally segmented deep brain stimulation leads for treating essential tremor. J Neural Eng 9 (4), 046005. doi: 10.1088/1741-2560/9/4/046005. PubMed DOI PMC

Kim JP, Min H−K, Knight EJ, et al., 2013. Centromedian-Parafascicular Deep Brain Stimulation Induces Differential Functional Inhibition of the Motor, Associative, and Limbic Circuits in Large Animals. Biol. Psychiatry 74 (12), 917–926. doi: 10.1016/j.biopsych.2013.06.024. PubMed DOI PMC

Kultas-Ilinsky K, Sivan-Loukianova E, Ilinsky IA, 2003. Reevaluation of the primary motor cortex connections with the thalamus in primates. J. Comp. Neurol 457 (2), 133–158. doi: 10.1002/cne.10539. PubMed DOI

Kuncel AM, Cooper SE, Wolgamuth BR, et al., 2006. Clinical response to varying the stimulus parameters in deep brain stimulation for essential tremor. Movement Disorders 21 (11), 1920–1928. doi: 10.1002/mds.21087. PubMed DOI

Lee J, Jo HJ, Kim I, et al., 2019. Mapping BOLD activation by pharmacologically evoked tremor in swine. Front Neurosci 13, 985. PubMed PMC

Lee KH, Chang S-Y, Jang D-P, et al., 2011. Emerging techniques for elucidating mechanism of action of deep brain stimulation. In: 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE, pp. 677–680. doi: 10.1109/IEMBS.2011.6090152. PubMed DOI PMC

Lehto LJ, Slopsema JP, Johnson MD, et al., 2017. Orientation selective deep brain stimulation. J Neural Eng 14 (1), 016016. doi: 10.1088/1741-2552/aa5238. PubMed DOI PMC

LeVan P, Gotman J, 2009. Independent component analysis as a model-free approach for the detection of BOLD changes related to epileptic spikes: a simulation study. Hum Brain Mapp 30 (7), 2021–2031. doi: 10.1002/hbm.20647. PubMed DOI PMC

Lozano AM, 2000. Vim thalamic stimulation for tremor. Arch. Med. Res 31 (3), 266–269. PubMed

Martens HC, Toader E, Decre MM, et al., 2011. Spatial steering of deep brain stimulation volumes using a novel lead design. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology 122 (3), 558–566. doi: 10.1016/j.clinph.2010.07.026. PubMed DOI

Mason A, Ilinsky IA, Beck S, Kultas-Ilinsky K, 1996. Reevaluation of synaptic relationships of cerebellar terminals in the ventral lateral nucleus of the rhesus monkey thalamus based on serial section analysis and three-dimensional reconstruction. Exp Brain Res 109 (2). doi: 10.1007/BF00231783. PubMed DOI

McIntyre CC, Mori S, Sherman DL, Thakor NV, Vitek JL, 2004. Electric field and stimulating influence generated by deep brain stimulation of the subthalamic nucleus. Clin Neurophysiol 115 (3), 589–595. doi: 10.1016/j.clinph.2003.10.033. PubMed DOI

Min H−K, Hwang S−C, Marsh MP, et al., 2012. Deep brain stimulation induces BOLD activation in motor and non-motor networks: an fMRI comparison study of STN and EN/GPi DBS in large animals. Neuroimage 63 (3), 1408–1420. doi: 10.1016/j.neuroimage.2012.08.006. PubMed DOI PMC

Moeller J, Strother S, Siditis J, Rottenberg D, 1987. The scaled subprofile model: a statistical approach to the analysis of functional patterns in positron emission tomographic data. J Cereb Blood Flow Metab 7, 649–658. PubMed

Moffitt MA, McIntyre CC, 2005. Model-based analysis of cortical recording with silicon microelectrodes. Clinical Neurophysiology 116 (9), 2240–2250. doi: 10.1016/j.clinph.2005.05.018. PubMed DOI

Paek SB, Min H−K, Kim I, et al., 2015a. Frequency-dependent functional neuromodulatory effects on the motor network by ventral lateral thalamic deep brain stimulation in swine. Neuroimage 105, 181–188. doi: 10.1016/j.neuroimage.2014.09.064. PubMed DOI PMC

Paek SB, Min H−K, Kim I, et al., 2015b. Frequency-dependent functional neuromodulatory effects on the motor network by ventral lateral thalamic deep brain stimulation in swine. Neuroimage 105, 181–188. doi: 10.1016/j.neuroimage.2014.09.064. PubMed DOI PMC

Papavassiliou E, Rau G, Heath S, et al., 2004. Thalamic Deep Brain Stimulation for Essential Tremor: relation of Lead Location to Outcome. Neurosurgery 54 (5), 1120–1130. doi: 10.1227/01.NEU.0000119329.66931.9E. PubMed DOI

Peña E, Zhang S, Deyo S, Xiao Y, Johnson MD, 2017. Particle swarm optimization for programming deep brain stimulation arrays. J Neural Eng 14 (1), 016014. doi: 10.1088/1741-2552/aa52d1. PubMed DOI PMC

Peña E, Zhang S, Patriat R, et al., 2018. Multi-objective particle swarm optimization for postoperative deep brain stimulation targeting of subthalamic nucleus pathways. J Neural Eng 15 (6), 066020. doi: 10.1088/1741-2552/aae12f. PubMed DOI PMC

Pollo C, Kaelin-Lang A, Oertel MF, et al., 2014. Directional deep brain stimulation: an intraoperative double-blind pilot study. Brain : a journal of neurology 137 (Pt 7), 2015–2026. doi: 10.1093/brain/awu102. PubMed DOI

Pouratian N, Reames DL, Frysinger R, Elias WJ, 2011. Comprehensive analysis of risk factors for seizures after deep brain stimulation surgery. Clinical article. J. Neurosurg 115 (2), 310–315. doi: 10.3171/2011.4.JNS102075. PubMed DOI

Rebelo P, Green AL, Aziz TZ, et al., 2018. Thalamic Directional Deep Brain Stimulation for tremor: spend less, get more. Brain Stimul 11 (3), 600–606. doi: 10.1016/j.brs.2017.12.015. PubMed DOI

Reker P, Dembek TA, Becker J, Visser-Vandewalle V, Timmermann L, 2016. Directional deep brain stimulation: a case of avoiding dysarthria with bipolar directional current steering. Parkinsonism Relat. Disord 31, 156–158. doi: 10.1016/j.parkreldis.2016.08.007. PubMed DOI

Richardson RM, Ostrem JL, Starr PA, 2009. Surgical Repositioning of Misplaced Subthalamic Electrodes in Parkinson’s Disease: location of Effective and Ineffective Leads. Stereotact Funct Neurosurg 87 (5), 297–303. doi: 10.1159/000230692. PubMed DOI

Ross EK, Kim JP, Settell ML, et al., 2016. Fornix deep brain stimulation circuit effect is dependent on major excitatory transmission via the nucleus accumbens. Neuroimage 128, 138–148. doi: 10.1016/j.neuroimage.2015.12.056. PubMed DOI PMC

Saikali S, Meurice P, Sauleau P, et al., 2010. A three-dimensional digital segmented and deformable brain atlas of the domestic pig. J. Neurosci. Methods 192 (1), 102–109. doi: 10.1016/j.jneumeth.2010.07.041. PubMed DOI

Sandvik U, Hariz G−M, Blomstedt P, 2012. Quality of life following DBS in the caudal zona incerta in patients with essential tremor. Acta Neurochir (Wien) 154 (3), 495–499. doi: 10.1007/s00701-011-1230-z. PubMed DOI

Schmidt C, van Rienen U, 2012. Modeling the Field Distribution in Deep Brain Stimulation: the Influence of Anisotropy of Brain Tissue. IEEE Transactions on Biomedical Engineering 59 (6), 1583–1592. doi: 10.1109/TBME.2012.2189885. PubMed DOI

Slopsema JP, Cass R, Hjelle M, Johnson MD, 2019. Advancing Directional Deep Brain Stimulation Array Technology. In: Proceedings of the 2019 Design of Medical Devices Conference 2019 Design of Medical Devices Conference Published online April.

Slopsema JP, Peña E, Patriat R, et al., 2018. Clinical deep brain stimulation strategies for orientation-selective pathway activation. J Neural Eng 15 (5), 056029. doi: 10.1088/1741-2552/aad978. PubMed DOI PMC

Springer, 2011. Molecular and Functional Models in Neuropsychiatry. Accessed September 10, 2019 http://public.eblib.com/choice/publicfullrecord.aspx?p=763654.

Steigerwald F, Müller L, Johannes S, Matthies C, Volkmann J, 2016. Directional deep brain stimulation of the subthalamic nucleus: a pilot study using a novel neurostimulation device. Movement Disorders 31 (8), 1240–1243. doi: 10.1002/mds.26669. PubMed DOI PMC

Teplitzky BA, Zitella LM, Xiao Y, Johnson MD, 2016. Model-Based Comparison of Deep Brain Stimulation Array Functionality with Varying Number of Radial Electrodes and Machine Learning Feature Sets. Front Comput Neurosci 58. doi: 10.3389/fncom.2016.00058, Published online. PubMed DOI PMC

Tracey DJ, Asanuma C, Jones EG, Porter R, 1980. Thalamic relay to motor cortex: afferent pathways from brain stem, cerebellum, and spinal cord in monkeys. J. Neurophysiol 44 (3), 532–554. PubMed

Vedam-Mai V, Krock N, Ullman M, et al., 2011. The national DBS brain tissue network pilot study: need for more tissue and more standardization. Cell Tissue Bank 12 (3), 219–231. doi: 10.1007/s10561-010-9189-1. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...