Dorsomedial prefontal cortex supports spontaneous thinking per se

Abstract

Spontaneous thinking, an action to produce, consider, integrate, and reason through mental representations, is central to our daily experience and has been suggested to serve crucial adaptive purposes. Such thinking occurs among other experiences during mind wandering that is associated with activation of the default mode network among other brain circuitries. Whether and how such brain activation is linked to the experience of spontaneous thinking per se remains poorly known. We studied 51 healthy subjects using a comprehensive experience-sampling paradigm during 3T functional magnetic resonance imaging. In comparison with fixation, the experiences of spontaneous thinking and spontaneous perception were related to activation of wide-spread brain circuitries, including the cortical midline structures, the anterior cingulate cortex and the visual cortex. In direct comparison of the spontaneous thinking versus spontaneous perception, activation was observed in the anterior dorsomedial prefrontal cortex. Modality congruence of spontaneous-experience-related brain activation was suggested by several findings, including association of the lingual gyrus with visual in comparison with non-verbal-non-visual thinking. In the context of current literature, these findings suggest that the cortical midline structures are involved in the integrative core substrate of spontaneous thinking that is coupled with other brain systems depending on the characteristics of thinking. Furthermore, involvement of the anterior dorsomedial prefrontal cortex suggests the control of high-order abstract functions to characterize spontaneous thinking per se. Hum Brain Mapp 38:3277-3288, 2017. © 2017 Wiley Periodicals, Inc.

Keywords: brain; cortical midline structures; default mode network; experience sampling; functional magnetic resonance imaging; human; thought.

Figure 1

Answer tree. Response options in the boxes were followed by further options as illustrated by the arrows. Asterisks represent options for psychotic experiences, which are a part of an on‐going patient study. Valence and arousal ratings were prompted for all thoughts on a continuous visual‐analog scale ranging from 0 to 100 (VAS).

Figure 2

Experiences during scanning. (A) Proportions for major experience classes. The narrow section represents 2% of experiences not falling into any of the defined categories. Here, the category “perception” also refers to experience of feelings in order to aid clarity. (B) Proportions of thought contents (C) The modality of non‐experiment‐related thinking (D) Proportions of percepts. The category “other” included feelings, bodily sensations, and visual and auditory perceptions of the surroundings.

Figure 3

Brain activation related to spontaneous experience of thinking (A) and (B) perception (pooled activation across specific categories in comparison with fixation; thresholded at voxelwise P < 0.005). White circles indicate the main regions of the default mode network following an automated meta‐analysis of 516 studies that included the key phrase “default mode” (Yarkoni et al., 2011). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Brain activation in the contrast “spontaneous thinking versus spontaneous perception.” Thresholded at voxelwise P < 0.005. Bars on the right present parameter estimates (mean and SEM) in the contrasts thinking versus fixation and perception versus fixation. The eigenvariates of parameter estimates were extracted from whole the dorsomedial region of interest to avoid any circularity in the analysis. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 5

Modality‐congruent brain activation during spontaneous experience (P < 0.005). (A) Lingual gyrus activation in the contrast “visual thought versus non‐visual–non‐verbal thought” (B) Auditory cortex activation in the contrast “scanner noise versus fixation” (C) Activation of the left anterior insula in the contrast of experiencing numbness or pressure (yellow) and needing to move (red) versus fixation. The need to move was also associated with activation of the supplementary motor area (D). [Color figure can be viewed at http://wileyonlinelibrary.com]