Case Report of Dual-Site Neurostimulation and Chronic Recording of Cortico-Striatal Circuitry in a Patient With Treatment Refractory Obsessive Compulsive Disorder

Sarah T Olsen, Ishita Basu, Mustafa Taha Bilge, Anish Kanabar, Matthew J Boggess, Alexander P Rockhill, Aishwarya K Gosai, Emily Hahn, Noam Peled, Michaela Ennis, Ilana Shiff, Katherine Fairbank-Haynes, Joshua D Salvi, Cristina Cusin, Thilo Deckersbach, Ziv Williams, Justin T Baker, Darin D Dougherty, Alik S Widge, Sarah T Olsen, Ishita Basu, Mustafa Taha Bilge, Anish Kanabar, Matthew J Boggess, Alexander P Rockhill, Aishwarya K Gosai, Emily Hahn, Noam Peled, Michaela Ennis, Ilana Shiff, Katherine Fairbank-Haynes, Joshua D Salvi, Cristina Cusin, Thilo Deckersbach, Ziv Williams, Justin T Baker, Darin D Dougherty, Alik S Widge

Abstract

Psychiatric disorders are increasingly understood as dysfunctions of hyper- or hypoconnectivity in distributed brain circuits. A prototypical example is obsessive compulsive disorder (OCD), which has been repeatedly linked to hyper-connectivity of cortico-striatal-thalamo-cortical (CSTC) loops. Deep brain stimulation (DBS) and lesions of CSTC structures have shown promise for treating both OCD and related disorders involving over-expression of automatic/habitual behaviors. Physiologically, we propose that this CSTC hyper-connectivity may be reflected in high synchrony of neural firing between loop structures, which could be measured as coherent oscillations in the local field potential (LFP). Here we report the results from the pilot patient in an Early Feasibility study (https://ichgcp.net/clinical-trials-registry/NCT03184454) in which we use the Medtronic Activa PC+ S device to simultaneously record and stimulate in the supplementary motor area (SMA) and ventral capsule/ventral striatum (VC/VS). We hypothesized that frequency-mismatched stimulation should disrupt coherence and reduce compulsive symptoms. The patient reported subjective improvement in OCD symptoms and showed evidence of improved cognitive control with the addition of cortical stimulation, but these changes were not reflected in primary rating scales specific to OCD and depression, or during blinded cortical stimulation. This subjective improvement was correlated with increased SMA and VC/VS coherence in the alpha, beta, and gamma bands, signals which persisted after correcting for stimulation artifacts. We discuss the implications of this research, and propose future directions for research in network modulation in OCD and more broadly across psychiatric disorders.

Keywords: cortico-striatal circuitry; local field potential; neural oscillations; neurostimulation; obsessive compulsive disorder; supplementary motor area; synchrony; ventral capsule/ventral striatum.

Copyright © 2020 Olsen, Basu, Bilge, Kanabar, Boggess, Rockhill, Gosai, Hahn, Peled, Ennis, Shiff, Fairbank-Haynes, Salvi, Cusin, Deckersbach, Williams, Baker, Dougherty and Widge.

Figures

FIGURE 1
FIGURE 1
Images of the DBS and paddle leads rendered with the Multi-Modality Visualization Tool (Felsenstein and Peled, 2017; Felsenstein et al., 2019). Position of left (red) and right (blue) SMA leads, and left (green) and right (yellow) VC/VS leads. Brodmann Area 6 is colored in turquoise. (A) coronal slice showing position of VC/VS leads (subcortical regions not colored). (B) Angled view with cortical coronal slice. Caudate nucleus colored in green, nucleus accumbens (Nacc) in blue, and putamen in pink. (C) Superior view (left on top) showing cortical lead positions. Note: the right VC/VS lead is in the caudate nucleus and NAcc whereas the left VC/VS lead is more laterally placed in the putamen. No adverse effects of lead placement were observed with the patient.
FIGURE 2
FIGURE 2
Figure depicts the timeline of study phases, changes in stimulation or recording parameters, and collection of clinical measures and LFP recordings. The x-axis values are days since the operation, and the ticks/labels denote days of clinical programming sessions. Note that there was no chronic cortical stimulation until day 235.
FIGURE 3
FIGURE 3
Schematic of saline bath preparation.
FIGURE 4
FIGURE 4
(A) Timing of important study events, for reference. (B) Clinical outcomes (from top to bottom YBOCS, MADRS, PGI, EMA) by days since operation.
FIGURE 5
FIGURE 5
Mean response time (in seconds) for each MSIT run as a function of day since operation the patient performed the task, collapsed across congruent and incongruent trials. Color of points indicates the stimulation phase: VC/VS only prior to setting optimization, VC/VS only after optimization, and combined VC/VS and cortical (100 Hz) stimulation.
FIGURE 6
FIGURE 6
Intraoperative WPLI as a function of VC/VS depth.
FIGURE 7
FIGURE 7
Average PSDs for: (A) the saline bath test (artifact) recordings; (B) the patient recordings prior to the removal of artifacts; and (C) the patient recordings after the subtraction of artifacts. For the patient recordings (B,C), each plot represents the recordings from each of the patient’s four leads, labeled by the brain region (cortical or VC/VS) and hemisphere. Plots in (A) (saline recordings) are labeled by which region and hemisphere a given recording matched in terms of recording and stimulation settings. Lines in each plot are the average PSD for all recordings, separated by the cortical stimulation frequency. Cortical stimulation frequency of 0 Hz indicates that no cortical stimulation was on during that recording. Lines represent means for all saline bath (A) or patient (B,C) recordings in each group. Error bands represent 95% confidence intervals, calculated from 1000 bootstrapped samples.
FIGURE 8
FIGURE 8
WPLI across frequency for: (A) the saline bath test (artifact) recordings; (B) the patient recordings prior to the removal of artifacts; and (C) the patient recordings after the subtraction of artifacts. Plots of patient recordings (B,C) indicate the cortical-striatal WPLI for the left and right hemispheres, with colored lines indicating the cortical stimulation frequency at the time of recording. Saline test plots (A) indicate whether the recording and stimulation settings for the IPGs matched those of the left or right hemisphere of patient recordings. Error bands represent 95% confidence intervals, calculated from 1000 bootstrapped samples.
FIGURE 9
FIGURE 9
(A) Timing of important study events for reference. (B) Heatmaps denoting the artifact corrected power (5–50 Hz) across the course of the study. (C) Artifact corrected cortical-striatal synchrony (WPLI) across the frequencies tested, as a function of days since operation. To better show subtle changes in WPLI, the range used for the color map is –0.1 to 0.2. Dotted lines on heatmaps (B,C) indicate clinical sessions, during which stimulation and recording settings changed and clinical outcomes were taken (see Figure 2 above for timing of important settings changes). Areas with missing LFP recordings have been interpolated (e.g., between days 138 and 151).
FIGURE 10
FIGURE 10
Correlations between YBOCS (A), MADRS (B), PGI (C), and EMA (D) and WPLI in the theta (leftmost column), alpha (second from the left), beta (second from the right), and gamma (rightmost column) bands. Data points are colored by the cortical stimulation frequency. Linear regressions (gray lines) were fit to the full data set for that measure (i.e., not separated by cortical stimulation frequency), with the error bands indicating the 95% confidence interval. Pearson correlations were also calculated, and the corresponding r and p-values are displayed.

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