The Phenomenal Contents and Neural Correlates of Spontaneous Thoughts across Wakefulness, NREM Sleep, and REM Sleep

Abstract

Thoughts occur during wake as well as during dreaming sleep. Using experience sampling combined with high-density EEG, we investigated the phenomenal qualities and neural correlates of spontaneously occurring thoughts across wakefulness, non-rapid eye movement (NREM) sleep, and REM sleep. Across all states, thoughts were associated with activation of a region of the midcingulate cortex. Thoughts during wakefulness additionally involved a medial prefrontal region, which was associated with metacognitive thoughts during wake. Phenomenologically, waking thoughts had more metacognitive content than thoughts during both NREM and REM sleep, whereas thoughts during REM sleep had a more social content. Together, these results point to a core neural substrate for thoughts, regardless of behavioral state, within the midcingulate cortex, and suggest that medial prefrontal regions may contribute to metacognitive content in waking thoughts.

Figure 1

The neural correlates of thoughts across wakefulness and sleep. Inflated cortical maps illustrating the cortical distribution of t values (two-tailed, paired t tests, p < .05, TFCE-corrected) for the contrast between trials with high thought and low thought at the source level for delta power (1–4 Hz) for (A) wakefulness (n = 13), (B) N2 sleep (n = 13), (C) REM sleep (n = 10). (D) Conjunction map showing the differences (yellow to orange) and overlap (red) of the topographical maps contrasting high-thought and low-thought trials across wakefulness, N2 sleep, REM sleep.

Figure 2

Metacognitive versus nonmetacognitive reports in wake. Inflated cortical map illustrating the topographical distribution of t values for the contrast between trials with no metacognition and metacognition at the source level for delta power (1–4 Hz) in wake (last 20 sec before the alarm sound). Only significant differences at the p < .05 level, obtained after correction for multiple comparisons, are shown (two-tailed, paired t tests, seven participants).