Imaging versus electrographic connectivity in human mood-related fronto-temporal networks

Joshua A Adkinson; Evangelia Tsolaki; Sameer A Sheth; Brian A Metzger; Meghan E Robinson; Denise Oswalt; Cameron C McIntyre; Raissa K Mathura; Allison C Waters; Anusha B Allawala; Angela M Noecker; Mahsa Malekmohammadi; Kevin Chiu; Richard Mustakos; Wayne Goodman; David Borton; Nader Pouratian; Kelly R Bijanki

doi:10.1016/j.brs.2022.03.002

Imaging versus electrographic connectivity in human mood-related fronto-temporal networks

Brain Stimul. 2022 May-Jun;15(3):554-565. doi: 10.1016/j.brs.2022.03.002. Epub 2022 Mar 12.

Authors

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

Affiliations

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.

Keywords: Connectivity; Cortico-cortical; DBS; Diffusion; Evoked potentials; Tractography.

Publication types

Research Support, N.I.H., Extramural

MeSH terms

Deep Brain Stimulation* / methods
Depressive Disorder, Treatment-Resistant* / therapy
Diffusion Tensor Imaging / methods
Gyrus Cinguli / physiology
Humans
White Matter* / physiology

Abstract

Publication types

MeSH terms

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