Time-frequency signatures evoked by single-pulse deep brain stimulation to the subcallosal cingulate

Ezra E Smith, Ki Sueng Choi, Ashan Veerakumar, Mosadoluwa Obatusin, Bryan Howell, Andrew H Smith, Vineet Tiruvadi, Andrea L Crowell, Patricio Riva-Posse, Sankaraleengam Alagapan, Christopher J Rozell, Helen S Mayberg, Allison C Waters, Ezra E Smith, Ki Sueng Choi, Ashan Veerakumar, Mosadoluwa Obatusin, Bryan Howell, Andrew H Smith, Vineet Tiruvadi, Andrea L Crowell, Patricio Riva-Posse, Sankaraleengam Alagapan, Christopher J Rozell, Helen S Mayberg, Allison C Waters

Abstract

Precision targeting of specific white matter bundles that traverse the subcallosal cingulate (SCC) has been linked to efficacy of deep brain stimulation (DBS) for treatment resistant depression (TRD). Methods to confirm optimal target engagement in this heterogenous region are now critical to establish an objective treatment protocol. As yet unexamined are the time-frequency features of the SCC evoked potential (SCC-EP), including spectral power and phase-clustering. We examined these spectral features-evoked power and phase clustering-in a sample of TRD patients (n = 8) with implanted SCC stimulators. Electroencephalogram (EEG) was recorded during wakeful rest. Location of electrical stimulation in the SCC target region was the experimental manipulation. EEG was analyzed at the surface level with an average reference for a cluster of frontal sensors and at a time window identified by prior study (50-150 ms). Morlet wavelets generated indices of evoked power and inter-trial phase clustering. Enhanced phase clustering at theta frequency (4-7 Hz) was observed in every subject and was significantly correlated with SCC-EP magnitude, but only during left SCC stimulation. Stimulation to dorsal SCC evinced stronger phase clustering than ventral SCC. There was a weak correlation between phase clustering and white matter density. An increase in evoked delta power (2-4 Hz) was also coincident with SCC-EP, but was less consistent across participants. DBS evoked time-frequency features index mm-scale changes to the location of stimulation in the SCC target region and correlate with structural characteristics implicated in treatment optimization. Results also imply a shared generative mechanism (inter-trial phase clustering) between evoked potentials evinced by electrical stimulation and evoked potentials evinced by auditory/visual stimuli and behavioral tasks. Understanding how current injection impacts downstream cortical activity is essential to building new technologies that adapt treatment parameters to individual differences in neurophysiology.

Keywords: deep brain stimulation; inter-trial phase clustering; perturbation mapping; single pulse electrical stimulation; stimulation evoked potential; subcallosal cingulate; time frequency analyses; treatment resistant depression (TRD).

Conflict of interest statement

HM received consulting and intellectual property licensing fees from Abbott Labs. KC received consulting fees from Abbott Labs. The terms approved by Emory University and the Icahn School of Medicine in accordance with policies to manage conflict of interest. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2022 Smith, Choi, Veerakumar, Obatusin, Howell, Smith, Tiruvadi, Crowell, Riva-Posse, Alagapan, Rozell, Mayberg and Waters.

Figures

FIGURE 1
FIGURE 1
Single pulse electrical stimulation of the subcallosal cingulate (SCC) target for deep brain stimulation. (A) Four contacts span the SCC target region on bilateral DBS electrodes. (B) EEG was recorded on the head surface during single pulse electrical stimulation at each contact on the DBS leads. (C) Analytic window was coincident with the SCC-EP (∼100 ms) detected in frontal channels.
FIGURE 2
FIGURE 2
Magnitude of unilateral stimulation evoked potentials increases along the ventral-to-dorsal axis of the SCC target region. (A) Grand average waveforms for stimulation-evoked potentials. Shaded areas depict 95% confidence intervals after 1,000 bootstraps. Left panel shows ERPs following left SCC stimulation, and right panel shows ERPs following right SCC stimulation. Topographic plots show ERP magnitude integrated over 50–150 ms time window. (B) Boxplots depicting average ERP amplitudes (averaged across 50–150 ms, electrode montage shown in Figure 1C) separately for stimulation location. Left panel shows averages for left-SCC stimulation, right panel shows averages for right-SCC stimulation.
FIGURE 3
FIGURE 3
ITPC at 4–7 Hz depends on location of DBS in the SCC region. (A) Spectrogram of ITPC across time and frequency. Box denotes time-frequency region-of-interest used for topographic plots. Left panel for left SCC stimulation, right panel for right SCC stimulation. (B) Box plots showing ITPC (50–150 ms, 4–7 Hz) at different stimulation locations. Left panel for left SCC stimulation, right panel for right SCC stimulation. Green = E0/8, Red = E1/9, Blue = E2/10, Black = E3/11.
FIGURE 4
FIGURE 4
ITPC at 4–7 Hz for individual participants. Spectrograms of average ITPC across all stimulation locations from frontal sensors (Figure 1C) for individual participants. Subject order (1–8) shown within panel: right to left column then top to bottom row. (A) Spectrograms show ITPC time-locked to left hemisphere SCC DBS, and (B) to right hemisphere SCC DBS. Stippled box denotes time-frequency region of interest used for group analysis and topographic plots in (B).
FIGURE 5
FIGURE 5
Topography and time course of ITPC at 4–7 Hz for individual participants. (A) ITPC topography for individual participants (4–7 Hz, 50–150 ms) averaged across all stimulation locations. The 8 topomaps on the left are from left SCC stimulation, and 8 topomaps on the right are from right SCC stimulation. Subject order (1–8) of topomaps: top rows (right to left) then bottom rows. (B) ITPC waveforms (4–7 Hz; frontal sensor montage, Figure 1C) from individual participants. Black lines are ITPC waveforms following stimulation at E3/11, green lines are ITPC waveforms following stimulation at E0/8. Left panel is from left SCC stimulation, and right panel is from right SCC stimulation.

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