Joshua A Adkinson1, Evangelia Tsolaki2, Sameer A Sheth3, Brian A Metzger4, Meghan E Robinson5, Denise Oswalt6, Cameron C McIntyre7, Raissa K Mathura8, Allison C Waters9, Anusha B Allawala10, Angela M Noecker11, Mahsa Malekmohammadi12, Kevin Chiu13, Richard Mustakos14, Wayne Goodman15, David Borton16, Nader Pouratian17, Kelly R Bijanki18. 1. Department of Neurosurgery, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. Electronic address: adkinson@bcm.edu. 2. Department of Neurosurgery, David Geffen School of Medicine at UCLA, 300 Stein Plaza Suite 562, Los Angeles, CA, 90095, USA. Electronic address: etsolaki@mednet.ucla.edu. 3. Department of Neurosurgery, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. Electronic address: sameer.sheth@bcm.edu. 4. Department of Neurosurgery, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. Electronic address: brian.metzger@bcm.edu. 5. Department of Neurosurgery, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. Electronic address: meghan.robinson@bcm.edu. 6. Department of Neurosurgery, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. Electronic address: denise.oswalt@bcm.edu. 7. Department of Biomedical Engineering, Case Western Reserve University, 10900 Euclid Ave., Cleveland, OH, 44106, USA. Electronic address: ccm4@case.edu. 8. Department of Neurosurgery, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. Electronic address: raissa.mathura@bcm.edu. 9. Department of Psychiatry, Mount Sinai School of Medicine, 1000 10th Ave., New York, NY, 10019, USA. Electronic address: allison.waters@mssm.edu. 10. School of Engineering, Brown University, 182 Hope St., Providence, RI, 02912, USA. Electronic address: anusha_allawala@brown.edu. 11. Department of Biomedical Engineering, Case Western Reserve University, 10900 Euclid Ave., Cleveland, OH, 44106, USA. Electronic address: amn6@case.edu. 12. Boston Scientific Neuromodulation, 25155 Rye Canyon Loop, Valencia, CA, 91355, USA. Electronic address: mahsa.malekmohammadi@bsci.com. 13. Brainlab, Inc., 5 Westbrook Corporate Center, Suite 1000, Westchester IL, 60154, USA. Electronic address: kevin.chiu@brainlab.com. 14. Boston Scientific Neuromodulation, 25155 Rye Canyon Loop, Valencia, CA, 91355, USA. Electronic address: richard.mustakos@bsci.com. 15. Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, 1977 Butler Blvd., Houston, TX, 77030, USA. Electronic address: wayne.goodman@bcm.edu. 16. School of Engineering, Brown University, 182 Hope St., Providence, RI, 02912, USA; Center for Neurorestoration and Neurotechnology, Rehabilitation R&D Service, Department of Veterans Affairs, Providence, RI, 02912, USA. Electronic address: daborton@brown.edu. 17. Department of Neurological Surgery, University of Texas Southwestern Medical Center, 8353 Harry Hines Blvd MC8855, Dallas, TX, 75239, USA. Electronic address: nader.pouratian@utsouthwestern.edu. 18. Department of Neurosurgery, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. Electronic address: bijanki@bcm.edu.
Abstract
BACKGROUND: The efficacy of psychiatric DBS is thought to be driven by the connectivity of stimulation targets with mood-relevant fronto-temporal networks, which is typically evaluated using diffusion-weighted tractography. OBJECTIVE: Leverage intracranial electrophysiology recordings to better predict the circuit-wide effects of neuromodulation to white matter targets. We hypothesize strong convergence between tractography-predicted structural connectivity and stimulation-induced electrophysiological responses. METHODS: Evoked potentials were elicited by single-pulse stimulation to two common DBS targets for treatment-resistant depression - the subcallosal cingulate (SCC) and ventral capsule/ventral striatum (VCVS) - in two patients undergoing DBS with stereo-electroencephalographic (sEEG) monitoring. Evoked potentials were compared with predicted structural connectivity between DBS leads and sEEG contacts using probabilistic, patient-specific diffusion-weighted tractography. RESULTS: Evoked potentials and tractography showed strong convergence in both patients in orbitofrontal, ventromedial prefrontal, and lateral prefrontal cortices for both SCC and VCVS stimulation targets. Low convergence was found in anterior cingulate (ACC), where tractography predicted structural connectivity from SCC targets but produced no evoked potentials during SCC stimulation. Further, tractography predicted no connectivity to ACC from VCVS targets, but VCVS stimulation produced robust evoked potentials. CONCLUSION: The two connectivity methods showed significant convergence, but important differences emerged with respect to the ability of tractography to predict electrophysiological connectivity between SCC and VCVS to regions of the mood-related network. This multimodal approach raises intriguing implications for the use of tractography in surgical targeting and provides new data to enhance our understanding of the network-wide effects of neuromodulation.
BACKGROUND: The efficacy of psychiatric DBS is thought to be driven by the connectivity of stimulation targets with mood-relevant fronto-temporal networks, which is typically evaluated using diffusion-weighted tractography. OBJECTIVE: Leverage intracranial electrophysiology recordings to better predict the circuit-wide effects of neuromodulation to white matter targets. We hypothesize strong convergence between tractography-predicted structural connectivity and stimulation-induced electrophysiological responses. METHODS: Evoked potentials were elicited by single-pulse stimulation to two common DBS targets for treatment-resistant depression - the subcallosal cingulate (SCC) and ventral capsule/ventral striatum (VCVS) - in two patients undergoing DBS with stereo-electroencephalographic (sEEG) monitoring. Evoked potentials were compared with predicted structural connectivity between DBS leads and sEEG contacts using probabilistic, patient-specific diffusion-weighted tractography. RESULTS: Evoked potentials and tractography showed strong convergence in both patients in orbitofrontal, ventromedial prefrontal, and lateral prefrontal cortices for both SCC and VCVS stimulation targets. Low convergence was found in anterior cingulate (ACC), where tractography predicted structural connectivity from SCC targets but produced no evoked potentials during SCC stimulation. Further, tractography predicted no connectivity to ACC from VCVS targets, but VCVS stimulation produced robust evoked potentials. CONCLUSION: The two connectivity methods showed significant convergence, but important differences emerged with respect to the ability of tractography to predict electrophysiological connectivity between SCC and VCVS to regions of the mood-related network. This multimodal approach raises intriguing implications for the use of tractography in surgical targeting and provides new data to enhance our understanding of the network-wide effects of neuromodulation.
Authors: Nikolaos Makris; Yogesh Rathi; Palig Mouradian; Giorgio Bonmassar; George Papadimitriou; Wingkwai I Ing; Edward H Yeterian; Marek Kubicki; Emad N Eskandar; Lawrence L Wald; Qiuyun Fan; Aapo Nummenmaa; Alik S Widge; Darin D Dougherty Journal: Brain Imaging Behav Date: 2016-12 Impact factor: 3.978
Authors: Donald A Malone; Darin D Dougherty; Ali R Rezai; Linda L Carpenter; Gerhard M Friehs; Emad N Eskandar; Scott L Rauch; Steven A Rasmussen; Andre G Machado; Cynthia S Kubu; Audrey R Tyrka; Lawrence H Price; Paul H Stypulkowski; Jonathon E Giftakis; Mark T Rise; Paul F Malloy; Stephen P Salloway; Benjamin D Greenberg Journal: Biol Psychiatry Date: 2008-10-08 Impact factor: 13.382
Authors: Darren L Clark; Kara A Johnson; Christopher R Butson; Catherine Lebel; David Gobbi; Rajamannar Ramasubbu; Zelma H T Kiss Journal: Brain Stimul Date: 2020-03-19 Impact factor: 8.955
Authors: Patricio Riva-Posse; Ki Sueng Choi; Paul E Holtzheimer; Cameron C McIntyre; Robert E Gross; Ashutosh Chaturvedi; Andrea L Crowell; Steven J Garlow; Justin K Rajendra; Helen S Mayberg Journal: Biol Psychiatry Date: 2014-04-13 Impact factor: 13.382
Authors: Chad J Donahue; Stamatios N Sotiropoulos; Saad Jbabdi; Moises Hernandez-Fernandez; Timothy E Behrens; Tim B Dyrby; Timothy Coalson; Henry Kennedy; Kenneth Knoblauch; David C Van Essen; Matthew F Glasser Journal: J Neurosci Date: 2016-06-22 Impact factor: 6.167
Authors: Himanshu Tyagi; Annemieke M Apergis-Schoute; Harith Akram; Tom Foltynie; Patricia Limousin; Lynne M Drummond; Naomi A Fineberg; Keith Matthews; Marjan Jahanshahi; Trevor W Robbins; Barbara J Sahakian; Ludvic Zrinzo; Marwan Hariz; Eileen M Joyce Journal: Biol Psychiatry Date: 2019-01-30 Impact factor: 13.382
Authors: David A Gutman; Paul E Holtzheimer; Timothy E J Behrens; Heidi Johansen-Berg; Helen S Mayberg Journal: Biol Psychiatry Date: 2008-11-14 Impact factor: 13.382