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Original Investigation | Circuits and Circuit Disorders

Mapping the “Depression Switch” During Intraoperative Testing of Subcallosal Cingulate Deep Brain Stimulation

Ki Sueng Choi, PhD1; Patricio Riva-Posse, MD1; Robert E. Gross, MD, PhD2; Helen S. Mayberg, MD1,3
[+] Author Affiliations
1Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, Georgia
2Department of Neurosurgery, Emory University School of Medicine, Atlanta, Georgia
3Department of Neurology, Emory University School of Medicine, Atlanta, Georgia
JAMA Neurol. 2015;72(11):1252-1260. doi:10.1001/jamaneurol.2015.2564.
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Importance  The clinical utility of monitoring behavioral changes during intraoperative testing of subcallosal cingulate deep brain stimulation is unknown.

Objective  To characterize the structural connectivity correlates of deep brain stimulation–evoked behavioral effects using probabilistic tractography in depression.

Design, Setting, and Participants  Categorization of acute behavioral effects was conducted in 9 adults undergoing deep brain stimulation implantation surgery for chronic treatment-resistant depression in a randomized and blinded testing session at Emory University. Patients were studied from September 1, 2011, through June 30, 2013. Post hoc analyses of the structural tractography patterns mediating distinct categories of evoked behavioral effects were defined, including the best response overall. Data analyses were performed from May 1 through July 1, 2015.

Main Outcomes and Measures  Categorization of stimulation-induced transient behavioral effects and delineation of the shared white matter tracts mediating response subtypes.

Results  Among the 9 patients, 72 active and 36 sham trials were recorded. The following stereotypical behavior patterns were identified: changes in interoceptive (noted changes in body state in 30 of 72 active and 4 of 36 sham trials) and in exteroceptive (shift in attention from patient to others in 9 of 72 active and 0 sham trials) awareness. The best response was a combination of exteroceptive and interoceptive changes at a single left contact for all 9 patients. Structural connectivity showed that the best response contacts had a pattern of connections to the bilateral ventromedial frontal cortex (via forceps minor and left uncinate fasciculus) and to the cingulate cortex (via left cingulum bundle), whereas behaviorally salient but nonbest contacts had only cingulate involvement. The involvement of the 3 white matter bundles during stimulation of the best contacts suggests a mechanism for the observed transient “depression switch.”

Conclusions and Relevance  This analysis of transient behavior changes during intraoperative deep brain stimulation of the subcallosal cingulate and the subsequent identification of unique connectivity patterns may provide a biomarker of a rapid-onset depression switch to guide surgical implantation and to refine and optimize algorithms for the selection of contacts in long-term stimulation for treatment-resistant depression.

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Figure 1.
Example of Deep Brain Stimulation Lead Location and Patient-Specific Volume of Tissue Activated (VTA) Used for Tractography Maps

The VTA seed (red ball) is shown in situ on a registered postoperative computed tomographic image. The anatomical location of the VTA is also seen on the superimposed high-resolution, T1-weighted magnetic resonance image. The size of the VTA seed is generated using the patient-specific stimulation settings shown (frequency, 130 Hz; pulse width, 90 microseconds; and stimulation amplitude, 6 mA). Contact numbers are designated C1 through C4.

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Figure 2.
Whole-Brain Probabilistic Tractography of a Shared Fiber Tract Map of Contacts With Best Intraoperative Responses

The following 3 common white matter bundles were affected by stimulation of the 9 left-sided contacts to mediate a best response: the uncinate fasciculus (UF) connecting to the ipsilateral ventromedial frontal cortex (A and C), the forceps minor (FM) connecting to the bilateral ventromedial frontal cortices (C and D), and the left cingulum bundle (CB) connecting to the ipsilateral anterior cingulate cortex (A, B, and D). Best response is described in the Intraoperative Behavior Response Assessments subsection of the Methods section. Blue labels indicate white matter bundles; black labels, cortical regions. ACC indicates anterior cingulate cortex; L, left side; MCC, midcingulate cortex; R, right side; SCC, subcallosal cingulate cortex; and vmF, ventromedial frontal cortex.

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Figure 3.
Whole-Brain Probabilistic Tractography of a Shared Fiber Tract Map of Contacts With Salient Intraoperative Responses

The common white matter bundle consists of the cingulum bundle (CB) connecting to ipsilateral anterior cingulate cortex. The images show the left (A and B) and right (C and D) hemisphere contacts with salient intraoperative response. Salient response is described in the Intraoperative Behavior Response Assessments subsection of the Methods section. Red labels indicate white matter bundles; black labels, cortical regions. ACC indicates anterior cingulate cortex; L, left side; R, right side; and SCC, subcallosal cingulate cortex.

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