Magnetoencephalographic correlates of mood and reward dynamics in human adolescents

Abstract

Despite its omnipresence in everyday interactions and its importance for mental health, mood and its neuronal underpinnings are poorly understood. Computational models can help identify parameters affecting self-reported mood during mood induction tasks. Here, we test if computationally modeled dynamics of self-reported mood during monetary gambling can be used to identify trial-by-trial variations in neuronal activity. To this end, we shifted mood in healthy (N = 24) and depressed (N = 30) adolescents by delivering individually tailored reward prediction errors while recording magnetoencephalography (MEG) data. Following a pre-registered analysis, we hypothesize that the expectation component of mood would be predictive of beta-gamma oscillatory power (25-40 Hz). We also hypothesize that trial variations in the source localized responses to reward feedback would be predicted by mood and by its reward prediction error component. Through our multilevel statistical analysis, we found confirmatory evidence that beta-gamma power is positively related to reward expectation during mood shifts, with localized sources in the posterior cingulate cortex. We also confirmed reward prediction error to be predictive of trial-level variations in the response of the paracentral lobule. To our knowledge, this is the first study to harness computational models of mood to relate mood fluctuations to variations in neural oscillations with MEG.

Keywords: MEG; mood; reward prediction error; reward processing.

Figure 1

Structure of the closed-loop gambling task. The gambling amounts are presented on the right side of the screen (in this example a possible win of 10 points or loss or − 10 points), while the certain choice (here a win of 1 point) is on the left. If choosing to gamble the certain amount disappears from the screen. The two possible gambling amounts are displayed on the screen for 4 s before the outcome is revealed (here a win of 10 points). There is a 2 s inter trial interval (ITI) before the start of the next trial. Every 2–3 trials participants are prompted to rate their mood. The mood question “How happy are you at this moment?” remains on the screen for 3 s before a sliding scale appears with the words “Unhappy” on the left end and “Happy” on the right, allowing participants to rate their mood with the FORP buttons.

Figure 2

Participants’ self-reported mood during the 3-blocks of the gambling task. Positive blocks have a white background while the negative block is shaded in gray. The left panel shows the average (n = 54) reported mood of all participants as a black line with standard deviation over subjects shaded in gray. The middle and right panels show, respectively, the average mood of all participants diagnosed with MDD (n = 30) and of all healthy volunteers (n = 24), with all individual reported moods shown as thinner black lines.

Figure 3

A. Maps of MEG sensors where the expectation parameter significantly predict beta-gamma power preceding mood rating in confirmatory sample. Sensors surviving clustering correction (, two-tailed, 10 000 random permutations) are shown in color. Color bar indicates t-statistic of the fixed effect. B. Source space maps showing brain regions where expectation predicts beta-gamma power preceding mood rating in confirmatory sample. Color bar indicates t-statistic of the fixed effect. Top row shows cluster peak in coronal and sagittal views. The plot on the bottom shows the significant cluster over multiple axial slices. Both predictors show similar significant clusters with a peak in the left posterior cingulate cortex (MNI coordinate [−2, −40, 30 mm) extending to mid cingulate, parietal cortex and the caudate.

Figure 4

Response to reward feedback in ROIs from the AAL atlas hypothesized to vary with mood or with the reward prediction error parameters. A. Response to feedback in the right insula cortex and prediction from self-reported mood. No significant temporal clusters were found in the confirmatory sample. B. ROIs with significant temporal clusters for the fixed effect. was confirmed to predict responses in right paracentral lobule (cluster peaks at 248 and 502 ms). No significant effect of was found in the right precuneus.

Figure 5

Expectation predicts the evoked response 250–400 ms after presentation of gambling options. A. Topographic map of the z-scored average MEG signal over all trials and subjects in the 250–400 ms time window after presentation of gambling options. B. Maps of MEG sensors where expectation parameter significantly predicts MEG response 250–400 ms following presentation of gambling options. Sensors surviving clustering correction (, two-tailed, 10 000 random permutations) are shown in color. Color bar indicates t-statistic of the fixed effect. Predictor did not show any surviving significant clusters. In source space. C. Time course of the evoked response (average over all trials and subjects in confirmatory sample) over all significant sensors (clusters in Fig. 5B). The time window of interest is highlighted in gray.

Figure 6

Subject level analysis: subject level expectation weight significantly (, 5000 random permutations) correlates with subject average beta-gamma power preceding mood rating. Color bar indicates Pearson’s correlation (r) for MEG power. Source map showing significantly correlated clusters has been masked with cortical and subcortical regions included in the AAL atlas. Subject beta-gamma power shows significant correlation clusters in subgenual ACC, caudate and occipital cortex. Voxels of overlap between MEG and fMRI results (Keren et al. 2021) are displayed in green and voxels where only fMRI showed significant correlation are in blue. Both modalities show a subject level brain activity correlating with in ACC regions.

Figure 7

Sensitivity analysis for beta-gamma power and the accumulated expectation . (A) Source clusters where expectation significantly predicts beta-gamma power in the sensitivity sample. (B) Multivariate analysis including fixed effect of group (HV or MDD) shows a reduced effect of with surviving clusters in the frontal cortex. (C) Significant effect of and MDD group interaction in the left temporal cortex.