Orientation selective deep brain stimulation of the subthalamic nucleus in rats

. 2020 Jun ; 213 () : 116750. [epub] 20200318

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32198048

Grantová podpora
P41 EB027061 NIBIB NIH HHS - United States
R01 NS094206 NINDS NIH HHS - United States
U01 NS103569 NINDS NIH HHS - United States

Deep brain stimulation (DBS) has become an important tool in the management of a wide spectrum of diseases in neurology and psychiatry. Target selection is a vital aspect of DBS so that only the desired areas are stimulated. Segmented leads and current steering have been shown to be promising additions to DBS technology enabling better control of the stimulating electric field. Recently introduced orientation selective DBS (OS-DBS) is a related development permitting sensitization of the stimulus to axonal pathways with different orientations by freely controlling the primary direction of the electric field using multiple contacts. Here, we used OS-DBS to stimulate the subthalamic nucleus (STN) in healthy rats while simultaneously monitoring the induced brain activity with fMRI. Maximal activation of the sensorimotor and basal ganglia-thalamocortical networks was observed when the electric field was aligned mediolaterally in the STN pointing in the lateral direction, while no cortical activation was observed with the electric field pointing medially to the opposite direction. Such findings are consistent with mediolateral main direction of the STN fibers, as seen with high resolution diffusion imaging and histology. The asymmetry of the OS-DBS dipolar field distribution using three contacts along with the potential stimulation of the internal capsule, are also discussed. We conclude that OS-DBS offers an additional degree of flexibility for optimization of DBS of the STN which may enable a better treatment response.

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Beck A, Teboulle M, 2009. Fast gradient-based algorithms for constrained total variation image denoising and deblurring problems. IEEE Trans Image Process 18, 2419–2434. PubMed

Benabid AL, Chabardes S, Mitrofanis J, Pollak P, 2009. Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson’s disease. Lancet Neurol 8, 67–81. PubMed

Bolam J, Hanley J, Booth P, Bevan M, 2000. Synaptic organisation of the basal ganglia. The Journal of Anatomy 196, 527–542. PubMed PMC

Boorman L, Kennerley AJ, Johnston D, Jones M, Zheng Y, Redgrave P, Berwick J, 2010. Negative blood oxygen level dependence in the rat: a model for investigating the role of suppression in neurovascular coupling. Journal of Neuroscience 30, 4285–4294. PubMed PMC

Butson CR, McIntyre CC, 2008. Current steering to control the volume of tissue activated during deep brain stimulation. Brain Stimul 1, 7–15. PubMed PMC

Calamante F, Tournier JD, Jackson GD, Connelly A, 2010. Track-density imaging (TDI): super-resolution white matter imaging using whole-brain track-density mapping. Neuroimage 53, 1233–1243. PubMed

Canteras NS, Shammah-Lagnado SJ, Silva BA, Ricardo JA, 1990. Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res 513, 43–59. PubMed

Castle M, Aymerich MS, Sanchez-Escobar C, Gonzalo N, Obeso JA, Lanciego JL, 2005. Thalamic innervation of the direct and indirect basal ganglia pathways in the rat: Ipsi- and contralateral projections. J Comp Neurol 483, 143–153. PubMed

Cavdar S, Ozgur M, Cakmak YO, Kuvvet Y, Kunt SK, Saglam G, 2018. Afferent projections of the subthalamic nucleus in the rat: emphasis on bilateral and interhemispheric connections. Acta Neurobiol Exp (Wars) 78, 251–263. PubMed

Chaturvedi A, Foutz TJ, McIntyre CC, 2012a. Current steering to activate targeted neural pathways during deep brain stimulation of the subthalamic region. Brain Stimul 5, 369–377. PubMed PMC

Chaturvedi A, Foutz TJ, McIntyre CC, 2012b. Current steering to activate targeted neural pathways during deep brain stimulation of the subthalamic region. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation 5, 369–377. PubMed PMC

Christen M, Bittlinger M, Walter H, Brugger P, Muller S, 2012. Dealing with side effects of deep brain stimulation: lessons learned from stimulating the STN. AJOB Neuroscience 3(1), 37–43 3, 37–43.

Clement EA, Richard A, Thwaites M, Ailon J, Peters S, Dickson CT, 2008. Cyclic and sleep-like spontaneous alternations of brain state under urethane anaesthesia. PLoS One 3, e2004. PubMed PMC

Coizet V, Graham JH, Moss J, Bolam JP, Savasta M, McHaffie JG, Redgrave P, Overton PG, 2009. Short-latency visual input to the subthalamic nucleus is provided by the midbrain superior colliculus. J Neurosci 29, 5701–5709. PubMed PMC

Contarino MF, Bour LJ, Verhagen R, Lourens MA, de Bie RM, van den Munckhof P, Schuurman PR, 2014. Directional steering: A novel approach to deep brain stimulation. Neurology 83, 1163–1169. PubMed

Field KJ, White WJ, Lang CM, 1993. Anaesthetic effects of chloral hydrate, pentobarbitone and urethane in adult male rats. Lab Anim 27, 258–269. PubMed

Flora ED, Perera CL, Cameron AL, Maddern GJ, 2010. Deep brain stimulation for essential tremor: a systematic review. Mov Disord 25, 1550–1559. PubMed

Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K, 2009. Optical Deconstruction of Parkinsonian Neural Circuitry. Science 324, 354. PubMed PMC

Hamani C, Florence G, Heinsen H, Plantinga BR, Temel Y, Uludag K, Alho E, Teixeira MJ, Amaro E, Fonoff ET, 2017. Subthalamic Nucleus Deep Brain Stimulation: Basic Concepts and Novel Perspectives. eNeuro 4. PubMed PMC

Hamani C, Saint-Cyr JA, Fraser J, Kaplitt M, Lozano AM, 2004. The subthalamic nucleus in the context of movement disorders. Brain 127, 4–20. PubMed

Horn A, Reich M, Vorwerk J, Li N, Wenzel G, Fang Q, Schmitz-Hubsch T, Nickl R, Kupsch A, Volkmann J, Kuhn AA, Fox MD, 2017. Connectivity Predicts deep brain stimulation outcome in Parkinson disease. Ann Neurol 82, 67–78. PubMed PMC

Howell B, Huynh B, Grill WM, 2015. Design and in vivo evaluation of more efficient and selective deep brain stimulation electrodes. J Neural Eng 12, 046030. PubMed PMC

Idiyatullin D, Corum C, Park JY, Garwood M, 2006. Fast and quiet MRI using a swept radiofrequency. J Magn Reson 181, 342–349. PubMed

Idiyatullin D, Corum CA, Garwood M, 2015. Multi-Band-SWIFT. J Magn Reson 251, 19–25. PubMed PMC

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, 046005. PubMed PMC

Kisely S, Hall K, Siskind D, Frater J, Olson S, Crompton D, 2014. Deep brain stimulation for obsessive-compulsive disorder: a systematic review and meta-analysis. Psychol Med 44, 3533–3542. PubMed

Kita T, Kita H, 2012. The subthalamic nucleus is one of multiple innervation sites for long-range corticofugal axons: a single-axon tracing study in the rat. J Neurosci 32, 5990–5999. PubMed PMC

Klinger NV, Mittal S, 2016. Clinical efficacy of deep brain stimulation for the treatment of medically refractory epilepsy. Clinical Neurology and Neurosurgery 140, 11–25. PubMed

Lai H-Y, Younce JR, Albaugh DL, Kao Y-CJ, Shih Y-YI, 2014. Functional MRI reveals frequency-dependent responses during deep brain stimulation at the subthalamic nucleus or internal globus pallidus. Neuroimage 84, 11–18. PubMed

Lai HY, Albaugh DL, Kao YCJ, Younce JR, Shih YYI, 2015. Robust deep brain stimulation functional MRI procedures in rats and mice using an MR-compatible tungsten microwire electrode. Magnetic resonance in medicine 73, 1246–1251. PubMed

Lakhan SE, Callaway E, 2010. Deep brain stimulation for obsessive-compulsive disorder and treatment-resistant depression: systematic review. BMC Res Notes 3, 60. PubMed PMC

Leemans A, Jeurissen B, Sijbers J, 2009. ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. in: 17th Annual Meeting of Intl Soc Mag Reson Med.

Lehto LJ, Filip P, Laakso H, Sierra A, Slopsema JP, Johnson MD, Eberly LE, Low WC, Grohn O, Tanila H, Mangia S, Michaeli S, 2018. Tuning Neuromodulation Effects by Orientation Selective Deep Brain Stimulation in the Rat Medial Frontal Cortex. Front Neurosci 12, 899. PubMed PMC

Lehto LJ, Idiyatullin D, Zhang J, Utecht L, Adriany G, Garwood M, Grohn O, Michaeli S, Mangia S, 2017a. MB-SWIFT functional MRI during deep brain stimulation in rats. Neuroimage 159, 443–448. PubMed PMC

Lehto LJ, Slopsema JP, Johnson MD, Shatillo A, Teplitzky BA, Utecht L, Adriany G, Mangia S, Sierra A, Low WC, 2017b. Orientation selective deep brain stimulation. Journal of neural engineering 14, 016016. PubMed PMC

Li Q, Ke Y, Chan DC, Qian ZM, Yung KK, Ko H, Arbuthnott GW, Yung WH, 2012. Therapeutic deep brain stimulation in Parkinsonian rats directly influences motor cortex. Neuron 76, 1030–1041. PubMed

Maggi CA, Meli A, 1986a. Suitability of urethane anesthesia for physiopharmacological investigations in various systems. Part 1: General considerations. Experientia 42, 109–114. PubMed

Maggi CA, Meli A, 1986b. Suitability of urethane anesthesia for physiopharmacological investigations in various systems. Part 2: Cardiovascular system. Experientia 42, 292–297. PubMed

Mallet L, Schupbach M, N’Diaye K, Remy P, Bardinet E, Czernecki V, Welter ML, Pelissolo A, Ruberg M, Agid Y, Yelnik J, 2007. Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior. Proc Natl Acad Sci U S A 104, 10661–10666. PubMed PMC

Martens HCF, Toader E, Decré MMJ, Anderson DJ, Vetter R, Kipke DR, Baker KB, Johnson MD, Vitek JL, 2011. Spatial steering of deep brain stimulation volumes using a novel lead design. Clinical neurophysiology 122, 558–566. PubMed

Min HK, Hwang SC, Marsh MP, Kim I, Knight E, Striemer B, Felmlee JP, Welker KM, Blaha CD, Chang SY, Bennet KE, Lee KH, 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, 1408–1420. PubMed PMC

Naito A, Kita H, 1994. The cortico-pallidal projection in the rat: an anterograde tracing study with biotinylated dextran amine. Brain Res 653, 251–257. PubMed

Okun MS, Fernandez HH, Wu SS, Kirsch-Darrow L, Bowers D, Bova F, Suelter M, Jacobson C.E.t., Wang X, Gordon CW Jr., Zeilman P, Romrell J, Martin P, Ward H, Rodriguez RL, Foote KD, 2009. Cognition and mood in Parkinson’s disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: the COMPARE trial. Ann Neurol 65, 586–595. PubMed PMC

Paasonen J, Stenroos P, Salo RA, Kiviniemi V, Grohn O, 2018. Functional connectivity under six anesthesia protocols and the awake condition in rat brain. Neuroimage 172, 9–20. PubMed

Pagliardini S, Funk GD, Dickson CT, 2013. Breathing and brain state: urethane anesthesia as a model for natural sleep. Respir Physiol Neurobiol 188, 324–332. PubMed

Phillips MD, Baker KB, Lowe MJ, Tkach JA, Cooper SE, Kopell BH, Rezai AR, 2006. Parkinson disease: pattern of functional MR imaging activation during deep brain stimulation of subthalamic nucleus--initial experience. Radiology 239, 209–216. PubMed

Pizzolato G, Mandat T, 2012. Deep brain stimulation for movement disorders. Front Integr Neurosci 6, 2. PubMed PMC

Plantinga BR, Roebroeck A, Kemper VG, Uludag K, Melse M, Mai J, Kuijf ML, Herrler A, Jahanshahi A, Ter Haar Romeny BM, Temel Y, 2016. Ultra-High Field MRI Post Mortem Structural Connectivity of the Human Subthalamic Nucleus, Substantia Nigra, and Globus Pallidus. Front Neuroanat 10, 66. PubMed PMC

Pollo C, Kaelin-Lang A, Oertel MF, Stieglitz L, Taub E, Fuhr P, Lozano AM, Raabe A, Schupbach M, 2014. Directional deep brain stimulation: an intraoperative double-blind pilot study. Brain 137, 2015–2026. PubMed

Rattay F, 1989. Analysis of models for extracellular fiber stimulation. IEEE Transactions on Biomedical Engineering 36, 676–682. PubMed

Rouzaire-Dubois B, Scarnati E, 1985. Bilateral corticosubthalamic nucleus projections: an electrophysiological study in rats with chronic cerebral lesions. Neuroscience 15, 69–79. PubMed

Schlegel F, Schroeter A, Rudin M, 2015. The hemodynamic response to somatosensory stimulation in mice depends on the anesthetic used: Implications on analysis of mouse fMRI data. Neuroimage 116, 40–49. PubMed

Schroeter A, Schlegel F, Seuwen A, Grandjean J, Rudin M, 2014. Specificity of stimulus-evoked fMRI responses in the mouse: the influence of systemic physiological changes associated with innocuous stimulation under four different anesthetics. Neuroimage 94, 372–384. PubMed

Shmuel A, Augath M, Oeltermann A, Logothetis NK, 2006. Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 9, 569–577. PubMed

Shmuel A, Yacoub E, Pfeuffer J, Van de Moortele PF, Adriany G, Hu X, Ugurbil K, 2002. Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 36, 1195–1210. PubMed

Slopsema JP, Pena E, Patriat R, Lehto LJ, Grohn O, Mangia S, Harel N, Michaeli S, Johnson MD, 2018. Clinical deep brain stimulation strategies for orientation-selective pathway activation. J Neural Eng 15, 056029. PubMed PMC

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, 1240–1243. PubMed PMC

Swanson LW, 2018. Brain maps 4.0—Structure of the rat brain: An open access atlas with global nervous system nomenclature ontology and flatmaps. Journal of Comparative Neurology 526, 935–943. PubMed PMC

Szabó I, Nád É, Szabó C, 1972. Pole reversals and hypothalamic self-stimulation: ascending spread of rewarding excitation. Physiology & behavior 9, 147–150. PubMed

Tommasi G, Krack P, Fraix V, Le Bas JF, Chabardes S, Benabid AL, Pollak P, 2008. Pyramidal tract side effects induced by deep brain stimulation of the subthalamic nucleus. J Neurol Neurosurg Psychiatry 79, 813–819. PubMed

Tournier JD, Calamante F, Connelly A, 2012. MRtrix: diffusion tractography in crossing fiber regions. International journal of imaging systems and technology 22(1), 53–66.

Van Den Berge N, Albaugh DL, Salzwedel A, Vanhove C, Van Holen R, Gao W, Stuber GD, Shih Y-YI, 2017. Functional circuit mapping of striatal output nuclei using simultaneous deep brain stimulation and fMRI. Neuroimage 146, 1050–1061. PubMed PMC

Van Den Honert C, Mortimer JT, 1979. Generation of unidirectionally propagated action potentials in a peripheral nerve by brief stimuli. Science 206, 1311–1312. PubMed

Xu W, Miocinovic S, Zhang J, Baker KB, McIntyre CC, Vitek JL, 2011. Dissociation of motor symptoms during deep brain stimulation of the subthalamic nucleus in the region of the internal capsule. Exp Neurol 228, 294–297. PubMed PMC

York MK, Dulay M, Macias A, Levin HS, Grossman R, Simpson R, Jankovic J, 2008. Cognitive declines following bilateral subthalamic nucleus deep brain stimulation for the treatment of Parkinson’s disease. J Neurol Neurosurg Psychiatry 79, 789–795. PubMed

Zaidel A, Spivak A, Grieb B, Bergman H, Israel Z, 2010. Subthalamic span of beta oscillations predicts deep brain stimulation efficacy for patients with Parkinson’s disease. Brain 133, 2007–2021. PubMed

Zhurakovskaya E, Paasonen J, Shatillo A, Lipponen A, Salo R, Aliev R, Tanila H, Grohn O, 2016. Global Functional Connectivity Differences between Sleep-Like States in Urethane Anesthetized Rats Measured by fMRI. PLoS One 11. PubMed PMC

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