Effects on resting-state EEG phase-amplitude coupling in insomnia disorder patients following 1 Hz left dorsolateral prefrontal cortex rTMS.
- Authors
- Guo, Yongjian; Zhao, Xumeng; Zhang, Xiaozi; Li, Minpeng; Liu, Xiaoyang; Lu, Ling; Liu, Jiayi; Li, Yan; Zhang, Shan; Yue, Lirong; Li, Jun; Liu, Jixin; Zhu, Yuanqiang; Zhu, Yifei; Sheng, Xiaona; Yu, Dahua; Yuan, Kai
- Year
- 2023
- Journal
- Human brain mapping
- PMID
- 36919444
- DOI
- 10.1002/hbm.26264
- PMCID
- PMC10171521
Despite burgeoning evidence for cortical hyperarousal in insomnia disorder, the existing results on electroencephalography spectral features are highly heterogeneous. Phase-amplitude coupling, which refers to the modulation of the low-frequency phase to a high-frequency amplitude, is probably a more sensitive quantitative measure for characterizing abnormal neural oscillations and explaining the therapeutic effect of repetitive transcranial magnetic stimulation in the treatment of patients with insomnia disorder. Sixty insomnia disorder patients were randomly divided into the active and sham treatment groups to receive 4 weeks of repetitive transcranial magnetic stimulation treatment. Behavioral assessments, resting-state electroencephalography recordings, and sleep polysomnography recordings were performed before and after repetitive transcranial magnetic stimulation treatment. Forty good sleeper controls underwent the same assessment. We demonstrated that phase-amplitude coupling values in the frontal and temporal lobes were weaker in Insomnia disorder patients than in those with good sleeper controls at baseline and that phase-amplitude coupling values near the intervention area were significantly enhanced after active repetitive transcranial magnetic stimulation treatment. Furthermore, the enhancement of phase-amplitude coupling values was significantly correlated with the improvement of sleep quality. This study revealed the potential of phase-amplitude coupling in assessing the severity of insomnia disorder and the efficacy of repetitive transcranial magnetic stimulation treatment, providing new insights on the abnormal physiological mechanisms and future treatments for insomnia disorder.
Experimental design and calculation process of PAC. (a) Experimental design. Sixty ID patients were randomly assigned to two groups to receive either active (n = 30) or sham (n = 30) rTMS treatment and received the same assessments before and after treatment. (b) The PAC calculation precess. The flow chart showed the evaluation process of PAC in detail.
Improvement of subjective and objective sleep efficiency after active rTMS treatment. Two‐way ANOVA revealed a significant “treatment × time” interaction effect in both subjective sleeping measurements (PSQI: F 56 = 24.14, p < .0001; ISI: F 56 = 18.34, p < .0001) and objective sleeping measurements (SE: F 45 = 7.265, p = .0099; NREM 3 duration: F 45 = 7.149, p = .0104; SOL: F 45 = 5.663, p = .0216). (a) Subjective sleep improvement was found by showing reduced PSQI (t 56 = 8.385, p < .0001) and ISI (t 56 = 6.962, p < .0001) in the active rTMS group. (b) Objective sleep improvement was found by showing increased sleep efficiency (t 45 = 2.539, p = .0291), NREM 3 duration (t 45 = 3.852, p = .0007), and shorter sleep onset latency (t 45 = 3.874, p = .0007) in the active rTMS group (ns = not significant, *p < .05; **p < .01; ***p < .001; ****p < .0001).
Differences in PAC values between GSC and ID patients at baseline (PAC values of GSC minus PAC values of ID patients), pink rectangles highlighted windows with significantly different PAC values using the cluster‐based permutation test (p corrected <.01) (Figure S2). The horizontal axis represents the frequency for phase and the vertical axis represents the frequency for amplitude. The unit is Hz.
Improvement of impaired PAC in ID patients after active rTMS. (a) Differences in PAC before and after active rTMS treatment (post minus pre), pink rectangles highlighted windows with significantly different PAC values before and after treatment using the cluster‐based permutation test (p corrected <.01) (Figure S3). (b) Differences in PAC values between ID patients and GSC. Histograms showed differences in PAC values of ID patients before and after active rTMS treatment. (c) Spatial distribution of electrodes where PAC were significantly difference. International standard 10‐20 EEG electrode distribution map showing significant differences in PAC electrode distribution in the vicinity of rTMS stimulation (yellow lightning represented stimulation target: F3). (d) Correlation between PAC values and sleep quality at baseline. Pearson correlation demonstrated that PAC values of F3, Fz, Cz, and T3 electrodes exhibited significant negative correlations with PSQI and ISI scores at baseline (ns = not significant, *p < .05; **p < 0.01; ***p < 0.001; ****p < 0.0001).
Correlation between elevated PAC and improved sleep quality and preferred phases at individual and group levels. (a) Correlation analysis showed that the change in PAC values (post–pre) on the Fz electrode was significantly negatively correlated with the change in sleep onset latency (post–pre). (b) Correlation analysis showed that the change in PAC on the F3 electrode (post–pre) was significantly negatively correlated with the change in SOL (post–pre). (c) Polar histograms show the individual‐ and group‐level preferred phases; the dark blue line represents the individual preferred phase, the red line represents the group average preferred phase, and the length of the line represents the coupling strength. Circular statistics showed that the PAC‐preferred phase of the Fz (5–7 Hz–50–56 Hz) electrode (pre‐rTMS: −2.00° ± 35.20°, post‐rTMS: −7.67° ± 29.70°, control: 4.59° ± 32.71°) was not significantly different between GSC and ID patients, and ID patients before and after active treatment (p > .05).
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