Spontaneous default network activity reflects behavioral variability independent of mind-wandering

Abstract

The brain's default mode network (DMN) is highly active during wakeful rest when people are not overtly engaged with a sensory stimulus or externally oriented task. In multiple contexts, increased spontaneous DMN activity has been associated with self-reported episodes of mind-wandering, or thoughts that are unrelated to the present sensory environment. Mind-wandering characterizes much of waking life and is often associated with error-prone, variable behavior. However, increased spontaneous DMN activity has also been reliably associated with stable, rather than variable, behavior. We aimed to address this seeming contradiction and to test the hypothesis that single measures of attentional states, either based on self-report or on behavior, are alone insufficient to account for DMN activity fluctuations. Thus, we simultaneously measured varying levels of self-reported mind-wandering, behavioral variability, and brain activity with fMRI during a unique continuous performance task optimized for detecting attentional fluctuations. We found that even though mind-wandering co-occurred with increased behavioral variability, highest DMN signal levels were best explained by intense mind-wandering combined with stable behavior simultaneously, compared with considering either single factor alone. These brain-behavior-experience relationships were highly consistent within known DMN subsystems and across DMN subregions. In contrast, such relationships were absent or in the opposite direction for other attention-relevant networks (salience, dorsal attention, and frontoparietal control networks). Our results suggest that the cognitive processes that spontaneous DMN activity specifically reflects are only partially related to mind-wandering and include also attentional state fluctuations that are not captured by self-report.

Keywords: daydreaming; default mode network; resting state; spontaneous thought; sustained attention.

Fig. S1.

Task paradigm. Subjects viewed gradually changing images of (frequent) city and (rare) mountain scenes. Subjects were instructed to respond with a button press to city but not mountain events. After 44–60 s, a self-paced thought-probe (bottom) appeared. Using a continuous scale (100, only else; 0, only task), subjects evaluated the degree to which they were just focused on the task or on something else just before appearance of the thought-probe.

Fig. S2.

Behavioral results. (A) Single-subject example of spontaneous fluctuations in self-reported attention (normalized off-task rating shown) and in prerating RT variance (absolute z averaged across 30-s prerating windows) across 36 thought-probes. (B) Average postscan ratings of the degree to which subjects reported attention off-task due to external distractions, task-related interferences, and mind-wandering (error bars denote SEM). (C) Within-subject Fisher-transformed Pearson correlations between off-task rating and ∼30-s prerating RT variance across 36 trial blocks within each subject (shaded dark gray denotes SEM; shaded light gray denotes SD; dark line denotes mean across subjects; dotted line demarcates zero value). Data points are slightly jittered along the x axis solely for visualization purposes. *P < 0.05, two-tailed Wilcoxon signed rank test. EDs, external distractions; MW, mind-wandering; RT, reaction time; TRIs, task-related interferences. (D) Correlations of interindividual differences in RT SD across all trial blocks vs. commission error rate across all trials (Left) and mean off-task rating across all thought-probes vs. average RT SD across all trial blocks (Middle) and vs. commission error rate across all trials (Right). RT, reaction.

Fig. 1.

DMN activity correlates positively with self-reported off-task attention and negatively with behavioral variability. (A) The DMN mask used for extracting mean activity, including cortical and cerebellar regions. (B) Within-subject Fisher-transformed Pearson correlations between prerating DMN %SC and off-task rating across 36 trial-blocks within each subject. (C) Within-subject Fisher-transformed Pearson correlations between prerating DMN %SC and prerating RT variance across 36 trial blocks within each subject. In B and C, shaded dark gray denotes SEM, shaded light gray denotes SD, dark line denotes mean across subjects, and dotted line demarcates zero value. *P < 0.05, two-tailed Wilcoxon signed rank test. DMN, default mode network; RT, reaction time; SC, signal change.

Fig. 2.

Self-reported attention and RT variability additively account for DMN activity. (A) 3D plot showing all trial blocks in all subjects with values for off-task rating (x₁; within-subject normalized off-task rating), RT variance (x₂), and DMN %SC (y). Color is proportional to mesh surface height, with red areas highest (high DMN activity) and blue areas lowest (low DMN activity). (B) Bar plots showing mean DMN %SC in trial blocks with four combinations of on-/off-task attention and high and low RT variance, with on/off (low/high) categories defined based on median split of all trial blocks of all subjects for within-subject normalized off-task ratings and RT variance. DMN, default mode network; RT, reaction time; SC, signal change.

Fig. 3.

DMN off-task relationship is driven most strongly by individuals with high relative levels of self-reported mind-wandering. The degree to which subjects reported off-task attention due to mind-wandering (relative to external distractions) is positively correlated with the within-subject Fisher-transformed Pearson correlation between off-task rating and prerating DMN %SC averaged within the 10-s prerating period. DMN, default mode network; SC, signal change.

Fig. S3.

Spearman’s ρ values for the analysis shown in Fig. 3 (based on DMN activity in 10 s), here repeated using single whole-brain volumes before and after the thought-probe onset (rather than averaging across brain volumes). Whole-brain volumes were acquired every 1.08 s. Because thought-probes were self-paced, the time between thought-probe onset and brain volume acquisition varied slightly from probe to probe. Thus, the TR numbers and corresponding time (s) on the x axis denote the upper limit of the possible time between thought-probe onset and volume acquisition (e.g., –2.16 s indicated on the plot denotes a range of –1.08 s to –2.16 s). DMN, default mode network; SC, signal change; TR, repetition time.

Fig. 4.

Subsystems of the DMN are associated with self-reported attention and RT variance. For each subsystem, we show within-subject Fisher-transformed Pearson correlations of prerating %SC with off-task rating (Left) and RT variance (Right) across 36 trial blocks within each subject. (A) The core DMN regions (yellow). (B) The dmPFC subsystem regions (blue). (C) The MTL subsystem regions (green). In all plots, shaded dark gray denotes SEM, shaded light gray denotes SD, dark line denotes mean across subjects, and dotted line demarcates zero value. *P < 0.05, two-tailed Wilcoxon signed rank test. DMN, default mode network; dmPFC, dorsomedial prefrontal cortex; MTL, medial temporal lobe; RT, reaction time; SC, signal change.

Fig. S4.

Correspondence of DMN areas associated with off-task attention and those associated with behavioral variability. (Top) Subregions of the DMN shown in different colors (54 total subregions). (Bottom) Plot of the correlation of %SC in a subregion with RT variance vs. the correlation of %SC with within-subject normalized off-task rating (r = –0.34, P = 0.01). Correlation values for each subregion were based on all trial blocks concatenated across all subjects. DMN, default mode network; ROI, region of interest; SC, signal change.

Fig. S5.

Correlations of salience, dorsal attention, frontoparietal control, and sensorimotor network activity with off-task ratings and with RT variance. The figure shows brain regions and plots of within-subject Fisher-transformed Pearson correlations of prerating network %SC with off-task rating (Left) and RT variance (Right) across 36 trial blocks within each subject for the (A) salience network (purple), (B) dorsal attention network (orange), (C) frontoparietal network (green), and (D) sensorimotor network (brown). In all plots, shaded dark gray denotes SEM, shaded light gray denotes SD, dark line denotes mean across subjects, dotted line demarcates zero value, and data points are slightly jittered along the x axis solely for visualization purposes. RT, reaction time; SC, signal change.