Increased theta/alpha synchrony in the habenula-prefrontal network with negative emotional stimuli in human patients
- Academy of Medical Engineering and Translational Medicine, Tianjin University, China
- Nuffield Department of Surgical Sciences, University of Oxford, United Kingdom
- Department of Neurosurgery, Affiliated Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, China
- Medical Research Council (MRC) Brain Network Dynamics Unit at the University of Oxford, Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom
Figures
Figure 1
Experimental paradigm and ratings (valence and arousal) of the presented pictures.
(A) Timeline of one individual trial: each trial started with a white cross (‘+’) presented with black background for 1 s, indicating the participants to get ready and pay attention; then a picture …
Figure 2
Electrode location and spectral characteristics of local field potentials from recorded habenula at rest.
(A) Electrode locations reconstructed using Lead-DBS, with the structures colored in light blue for the habenula, purple for the caudate nucleus, light green for the red nucleus, and yellow for …
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Figure 2—source data 1
Source data for generating Figure 2B, C.
- https://cdn.elifesciences.org/articles/65444/elife-65444-fig2-data1-v1.mat
Figure 3 with 2 supplements
Habenular theta/alpha activity is differentially modulated by stimuli with positive and negative emotional valence (N = 18 habenula local field potential samples from nine subjects).
(A–C) Time-frequency representations of the power response relative to pre-stimulus baseline (−2000 to −200 ms) for neutral (A), positive (B), and negative (C) valence stimuli, respectively. …
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Figure 3—source data 1
Source data for generating Figure 3.
- https://cdn.elifesciences.org/articles/65444/elife-65444-fig3-data1-v1.mat
Figure 3—figure supplement 1
Event-related potential (ERP) in habenula local field potential signals in different emotional valence (neutral, positive, and negative) conditions.
(A) Averaged ERP waveforms across patients for different conditions. (B) Peak latency and amplitude (mean ± SEM) of the ERP components for different conditions.
Figure 3—figure supplement 2
Non-phase-locked (induced only) activity in different emotional valence (neutral, positive, and negative) conditions (N = 18).
(A) Time-frequency representation of the power changes relative to pre-stimulus baseline for three conditions. Significant clusters (p<0.05, non-parametric permutation test) are encircled with a …
Figure 4
Theta/alpha oscillations in the prefrontal cortex are differentially modulated by stimuli with positive and negative emotional valence (N = 8 magnetoencephalography [MEG] samples from eight subjects).
(A) Layout of the MEG sensor positions and selected frontal sensors (dark spot). (B) Time-frequency representation of the power changes relative to pre-stimulus baseline for neutral, positive, and …
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Figure 4—source data 1
Source data for generating Figure 4.
- https://cdn.elifesciences.org/articles/65444/elife-65444-fig4-data1-v1.mat
Figure 5 with 1 supplement
Statistical source maps of t-values (p<0.05; corrected for whole brain) for the comparison of magnetoencephalography (MEG) theta/alpha band (5–10 Hz) power reactivity to negative vs. positive emotional valence stimuli across subjects (N = 8 MEG samples from eight subjects).
Dynamic imaging of coherent source beamformer was applied to the average theta/alpha band power changes from 100 to 500 ms after stimulus onset. The image was transformed to MNI template space and …
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Figure 5—source data 1
Source data for generating Figure 5.
- https://cdn.elifesciences.org/articles/65444/elife-65444-fig5-data1-v1.zip
Figure 5—figure supplement 1
An example of dynamic imaging of coherent source (DICS) beamforming for the movement-related beta power source localization in one participant (Case 8).
(A) Time-frequency maps of magnetoencephalography activity for right-hand button press at sensor level from one participant. (B) DICS beamforming source reconstruction of the areas with …
Figure 6 with 1 supplement
Cortical-habenular coherence in the theta/alpha band is also differentially modulated by stimuli with positive and negative emotional valence (N = 16 local field potential-magnetoencephalography [LFP-MEG] combination samples from eight subjects).
(A) Time-varying theta (5–10 Hz) habenula-cortical coherence changes relative to pre-cue baseline averaged across all MEG channel combinations for each recorded habenula. The thick colored lines and …
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Figure 6—source data 1
Source data for generating Figure 6.
- https://cdn.elifesciences.org/articles/65444/elife-65444-fig6-data1-v1.zip
Figure 6—figure supplement 1
Time-varying coherence changes for frontal cortex-habenula and occipital cortex-habenula separately.
(A) Time-varying theta (5–10 Hz) habenula-cortical coherence changes relative to pre-cue baseline averaged across habenula-frontal magnetoencephalography (MEG) channel combinations for each …
Figure 7
Scatter plots showing how early theta/alpha band power increase in the frontal cortex (A) theta/alpha band frontal cortex-habenula coherence (B) and theta band power increase at a later time window in habenula (C) changed with emotional valence (left column) and arousal (right column).
Each dot shows the average of one participant in each categorical valence condition, which are also the source data of the multilevel modeling results presented in Table 2. The estimated correlation …
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Figure 7—source data 1
- https://cdn.elifesciences.org/articles/65444/elife-65444-fig7-data1-v1.mat
Tables
Table 1
Characteristics of enrolled subjects.
| Patient | Sex | Age (years) | Duration (years) | Disease | HAMD score | BDI score | Resting oscillation peaks | |
|---|---|---|---|---|---|---|---|---|
| L | R | |||||||
| 1 | M | 21 | 5 | Schiz | NA | 32 | 9.1 Hz | 9.8 Hz |
| 2 | M | 21 | 5 | Dep | 12 | 10 | 7.9 Hz | 8.4 Hz |
| 3 | M | 44 | 10 | Bipolar | 23 | 22 | 14.3 Hz | 15.9 Hz |
| 4 | F | 19 | 4 | Schiz | NA | NA | 10 Hz | 8.1 Hz |
| 5 | M | 21 | 3 | Dep | 24 | 38 | 7.1 Hz | 16.9 Hz |
| 6 | M | 16 | 2 | Schiz | NA | 34 | 9.2 Hz; 13.0 Hz | 7.2 Hz; 12.5 Hz |
| 7 | F | 30 | 8 | Bipolar | 21 | 33 | 6.1 Hz | 7.8 Hz |
| 8 | F | 28 | 13 | Dep | 28 | 37 | No peak | 8.0 Hz |
| 9 | M | 35 | 20 | Dep | 25 | 34 | 16.2 Hz | 7.9 Hz; 16.0 Hz |
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Hab: habenula; F: female; M: male; Dep: depressive disorder; Bipolar: bipolar disorder; Schiz: schizophrenia; HAMD: Hamilton Depression Rating Scale (17 items); BDI: Beck Depression Inventory; Both HAMD and BDI were acquired before the surgery. NA: not available.
Table 2
Linear mixed effect modeling details.
| ID | Model | Fixed effect of valence | Fixed effect of arousal | R2 | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| k-Value | 95% CI | p-Value | k-Value | 95% CI | p-Value | |||||||
| 1 | HabTheta1∼ Valence+Arousal+1|SubID | −2.8044 ± 0.9840 | [−4.7800,–0.8289] | 0.0063 | −2.5221 ± 2.5363 | [−7.6139, 2.5697] | 0.3247 | 0.6191 | ||||
| 2 | HabTheta2∼ Valence+Arousal+1|SubID | −4.4526 ± 1.1753 | [−6.8121,–2.0932] | 0.0004 | 0.1975 ± 3.0295 | [−5.8844, 6.2794] | 0.9483 | 0.2557 | ||||
| 3 | PFC_Theta∼ Valence+Arousal+1|SubID | −2.8921 ± 1.0221 | [−4.9507,–0.8334] | 0.0069 | −3.6237 ± 2.6252 | [−8.9112, 1.6637] | 0.1743 | 0.4368 | ||||
| 4 | rPFC_Hab_Coh∼ Valence+Arousal+1|SubID | −6.1031 ± 1.6785 | [−9.4837,–2.7225] | 0.0007 | 3.5242 ± 4.3112 | [−5.1589, 12.2074] | 0.4180 | 0.2766 | ||||
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HabTheta1: theta/alpha band (5–10 Hz) in habenula LFPs at 100–500 ms ; HabTheta2: theta band (4–7 Hz) in habenula LFPs at 2700–3300 ms; PFC_Theta: theta/alpha band (5–10 Hz) averaged across frontal sensors at 100–500 ms; rPFC_Hab_Coh: theta/alpha band (5–10 Hz) coherence between right PFC and habenula at 800–1300 ms; Valence: valence value for the displayed pictures (1 = unpleasant -> 5 = neutral -> 9 = pleasant); Arousal: arousal value of the displayed pictures (1 = calm -> 9 = exciting); LFP: local field potential; PFC: prefrontal cortex.
Additional files
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Source code 1
The source code file is a compressed folder containing the MATLAB scripts to generate the figures and separate files for the source data to generate different figures with the file names indicating the figure or table with which the data was associated.
- https://cdn.elifesciences.org/articles/65444/elife-65444-code1-v1.zip
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Transparent reporting form
- https://cdn.elifesciences.org/articles/65444/elife-65444-transrepform-v1.docx
