Coordinated Reset Vibrotactile Stimulation Induces Sustained Cumulative Benefits in Parkinson's Disease

Kristina J Pfeifer, Justus A Kromer, Alexander J Cook, Traci Hornbeck, Erika A Lim, Bruce J P Mortimer, Adam S Fogarty, Summer S Han, Rohit Dhall, Casey H Halpern, Peter A Tass, Kristina J Pfeifer, Justus A Kromer, Alexander J Cook, Traci Hornbeck, Erika A Lim, Bruce J P Mortimer, Adam S Fogarty, Summer S Han, Rohit Dhall, Casey H Halpern, Peter A Tass

Abstract

Background: Abnormal synchronization of neuronal activity in dopaminergic circuits is related to motor impairment in Parkinson's disease (PD). Vibrotactile coordinated reset (vCR) fingertip stimulation aims to counteract excessive synchronization and induce sustained unlearning of pathologic synaptic connectivity and neuronal synchrony. Here, we report two clinical feasibility studies that examine the effect of regular and noisy vCR stimulation on PD motor symptoms. Additionally, in one clinical study (study 1), we examine cortical beta band power changes in the sensorimotor cortex. Lastly, we compare these clinical results in relation to our computational findings.

Methods: Study 1 examines six PD patients receiving noisy vCR stimulation and their cortical beta power changes after 3 months of daily therapy. Motor evaluations and at-rest electroencephalographic (EEG) recordings were assessed off medication pre- and post-noisy vCR. Study 2 follows three patients for 6+ months, two of whom received daily regular vCR and one patient from study 1 who received daily noisy vCR. Motor evaluations were taken at baseline, and follow-up visits were done approximately every 3 months. Computationally, in a network of leaky integrate-and-fire (LIF) neurons with spike timing-dependent plasticity, we study the differences between regular and noisy vCR by using a stimulus model that reproduces experimentally observed central neuronal phase locking.

Results: Clinically, in both studies, we observed significantly improved motor ability. EEG recordings observed from study 1 indicated a significant decrease in off-medication cortical sensorimotor high beta power (21-30 Hz) at rest after 3 months of daily noisy vCR therapy. Computationally, vCR and noisy vCR cause comparable parameter-robust long-lasting synaptic decoupling and neuronal desynchronization.

Conclusion: In these feasibility studies of eight PD patients, regular vCR and noisy vCR were well tolerated, produced no side effects, and delivered sustained cumulative improvement of motor performance, which is congruent with our computational findings. In study 1, reduction of high beta band power over the sensorimotor cortex may suggest noisy vCR is effectively modulating the beta band at the cortical level, which may play a role in improved motor ability. These encouraging therapeutic results enable us to properly plan a proof-of-concept study.

Keywords: Parkinson’s disease; beta band power; coordinated reset; cumulative effects; desynchronization; sensorimotor; vibrotactile stimulation.

Conflict of interest statement

TH works as consultant for Boston Scientific and received teaching honoraria for DBS courses. RD has served as a clinical trials investigator for Impax Pharmaceuticals, Pharma2B, CALA Health, Axovant and Neurocrine Biosciences. CH has received speaking honoraria and consulting fees from Boston Scientific, Medtronic, and NeuroPace. PT works as consultant for Boston Scientific Neuromodulation and Gretap AG and is inventor on a number of patents for non-invasive neuromodulation. BM is employed by Engineering Acoustics who manufacture vibrotactile systems. No further disclosures. 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 © 2021 Pfeifer, Kromer, Cook, Hornbeck, Lim, Mortimer, Fogarty, Han, Dhall, Halpern and Tass.

Figures

FIGURE 1
FIGURE 1
Stimulation patterns used throughout the paper. (A) Regular 3:2 ON-OFF coordinated reset with rapidly varying sequence (CR RVS) pattern. (B) Noisy 3:2 ON-OFF CR RVS pattern and 23.5% jitter. (C) Purely periodic multichannel stimulation. Gray lines indicate multiples of the vibrotactile coordinated reset (vCR) period TCR, and dotted lines indicate multiples of TCR/4 during individual CR periods. Roman numerals indicate fingertips on one hand. Stimulation bursts are marked red. Red vertical lines indicate maxima of fvib(t), Eq. (2), during individual bursts. Parameters: fCR = 1.5 Hz (TCR4 = 166.7 ms), burst duration 100 ms, and fburst = 250 Hz.
FIGURE 2
FIGURE 2
Study procedures were as follows: 1–2 weeks before the first visit, while on medication, Parkinson’s disease (PD) patients took the Movement Disorders Society-Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) parts 1,2, and 4, Parkinson’s Disease Questionnaire-39 (PDQ-39), Scales for Outcomes in Parkinson’s Disease-COGnition (SCOPA-COG) and reported levodopa equivalent daily dose (LEDD). On the first visit, PD patients were off medication and the MDS-UPDRS 3 was administered, followed by an at-rest electroencephalography (EEG). Patients withdrew their medication again overnight and on day 2 patients were assessed with a morning MDS-UPDRS part 3, followed by 2 × 2 h of vibrotactile coordinated reset (vCR) stimulation and then an afternoon MDS-UPDRS part 3 (directly after 4 h of stimulation) to assess acute effects of vCR. After day 2, patients were instructed at home to do 2 h of vCR treatment in the morning and 2 h in the afternoon or night. The assessments described above were then repeated at 3 months of vCR treatment.
FIGURE 3
FIGURE 3
Yellow highlighted areas indicate selected electrodes for source estimation. Data from electrodes near or on the cheeks or close to the nape of the neck were removed to reduce noise. Vertical (E18, E37) and lateral (E252, E226) eye electrodes are highlighted in green.
FIGURE 4
FIGURE 4
The yellow highlighted region of the Schaefer 200 parcellation map (Schaefer et al., 2018) represents the somatomotor A region of interest (ROI). This ROI was used for source analysis.
FIGURE 5
FIGURE 5
(A) On the first visit, Parkinson’s disease (PD) patients displayed a significant acute effect for vibrotactile coordinated reset (vCR) treatment. Specifically, Movement Disorders Society-Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) III pretreatment scores (M = 39.833, SD = 11.14) significantly decreased after 4 h of stimulation (M = 31.833, SD = 9.38). (B) Additionally, MDS-UPDRS III pretreatment scores (M = 38.33 ± 7.86) significantly decreased after 3 months of vCR treatment (M = 32.33, SD = 7.80). Panel (C) represents baseline (M = 45, SD = 9.89) and 3-month (M = 34, SD = 9.89) MDS-UPDRS III data for the two patients in study 2 who received regular vCR. While no statistics can be used due to the small sample size, regular vCR results are represented visuallyfor comparison to the noisy vCR results. Regardless of vCR type, these findings suggest significant improvement of motor ability. Panels (A,B) show box plots, whereas the boxes in panel (C) simply comprise the two patients’ values.
FIGURE 6
FIGURE 6
To assess clinical significance of acute and cumulative treatment outcomes, minimal clinically important differences (MCID = –3.25) were compared to Movement Disorders Society-Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) score changes [i.e., Delta MDS-UPDRS III = post-vibrotactile coordinated reset (vCR) MDS-UPDRS III minus pre-vCR MDS-UPDRS III] obtained by subtracting pretreatment (baseline) vCR MDS-UPDRS III scores from posttreatment vCR MDS-UPDRS III scores on the first visit to measure acute effects (green bars) and by subtracting pretreatment (baseline) vCR MDS-UPDRS III scores from posttreatment vCR MDS-UPDRS III scores after 3 months of vCR treatment to measure cumulative effects (orange bars). For acute effects measured on the first visit, five out of six patients were able to clinically reduce MDS-UPDRS III after 4 h of vCR treatment. Additionally, all patients showed a clinically significant reduction of MDS-UPDRS III scores after 3 months of vCR treatment.
FIGURE 7
FIGURE 7
Displays relative power for the high beta (21–30 Hz) band in the somatomotor A region. At-rest recordings revealed that the sensorimotor region on day 1 pre-vibrotactile coordinated reset (vCR) (A) (M = 0.079 ± 0.036) significantly decreased in high beta relative power after 3 months of vCR treatment (B) (M = 0.058 ± 0.025).
FIGURE 8
FIGURE 8
Displays cumulative chronic, months-long effects of vibrotactile coordinated reset (vCR) treatment. For all three patients, significant negative correlations for the Movement Disorders Society-Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) III were found [Patient 1 (A), r = –0.744, p = 0.001; Patient 2 (B), r = –0.998, p = 0.002; Patient 3 (C), r = –0.992, p = 0.001). Patient 3 (C) also exhibited a slight decrease in MDS-UPDRS III scores at the preplanned 1-month pause in stimulation between 6 and 7 months. These results suggest significant improvement of motor ability.
FIGURE 9
FIGURE 9
Stimulation shapes neuronal spiking activity. Raster plots of neuronal spiking activity during the first few seconds of vibrotactile stimulation with a regular vibrotactile coordinated reset (vCR) pattern (A), a noisy vCR pattern (same sequence as regular CR but with jitter of 23.5%) (B), and vibratory purely periodic multichannel stimulation (vPPMS) (C). Sensory inputs caused by vibratory burst delivery to corresponding fingertips are marked red. Parameters: t = 0 marks onset of stimulation with fCR = 1.67 Hz and A = A0.
FIGURE 10
FIGURE 10
Long-lasting desynchronization by sensory stimulation with noisy vibrotactile coordinated reset (vCR). (A) Time trace of the Kuramoto order parameter ρ(t) and the mean synaptic weight ⟨w⟩(t) before, during (red), and after noisy vCR stimulation. (B) Snapshots of connectivity matrices containing the values of all synaptic weights wi→j(t) evaluated at indicated times after onset of stimulation; see also labels in panel (A). Parameters: J = 23.5%, fCR = 1.5 Hz, and A = A0.
FIGURE 11
FIGURE 11
Parameter dependence of stimulation-induced desynchronization and weight dynamics in the neuronal network model. (A–C) Acute effects of regular vibrotactile coordinated reset (vCR) (A), noisy vCR (B), and vibratory purely periodic multichannel stimulation (vPPMS) (C). Columns show results for the acute Kuramoto order parameter ρac evaluated shortly before stimulation ceases (first column); the corresponding mean synaptic weight wac (second column); and mean weights of intrapopulation (third column) and interpopulation synapses (fourth column), respectively. (D–F) Corresponding long-lasting effects of regular vCR (D), noisy vCR (E), and vPPMS (F) evaluated 1 h after cessation of stimulation. Here, the first column shows the Kuramoto order parameter ρll and the second column the mean synaptic weight wll. For comparison, the mean period of the original synchronous rhythm (1/fsynch,fsynch = 286 ms) is marked by vertical dashed red lines. All results were time-averaged over an interval of 12 s shortly before cessation of stimulation (A–C) and 1 h after cessation of stimulation (D–F). Data points show ensemble averages (marked by angular brackets) over five network and sequence realizations. Results for noisy vCR were obtained using a jitter of 23.5%.

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