Elsevier

NeuroImage

Volume 146, 1 February 2017, Pages 226-235
NeuroImage

Individual variation in intentionality in the mind-wandering state is reflected in the integration of the default-mode, fronto-parietal, and limbic networks

https://doi.org/10.1016/j.neuroimage.2016.11.025Get rights and content

Highlights

  • Deliberate and spontaneous mind-wandering have unique structural and functional correlates.

  • Reports of deliberate mind-wandering correlated with regions in both default-mode and fronto-parietal networks.

  • Spontaneous mind-wandering was linked to less integrity in parietal and temporal regions.

  • Intentionality during the mind-wandering state may depend upon integration between the default-mode and fronto-parietal networks.

  • These neurocognitive differences explain why mind-wandering has a complex relationship with cognitive control.

Abstract

Mind-wandering has a controversial relationship with cognitive control. Existing psychological evidence supports the hypothesis that episodes of mind-wandering reflect a failure to constrain thinking to task-relevant material, as well the apparently alternative view that control can facilitate the expression of self-generated mental content. We assessed whether this apparent contradiction arises because of a failure to consider differences in the types of thoughts that occur during mind-wandering, and in particular, the associated level of intentionality. Using multi-modal magnetic resonance imaging (MRI) analysis, we examined the cortical organisation that underlies inter-individual differences in descriptions of the spontaneous or deliberate nature of mind-wandering. Cortical thickness, as well as functional connectivity analyses, implicated regions relevant to cognitive control and regions of the default-mode network for individuals who reported high rates of deliberate mind-wandering. In contrast, higher reports of spontaneous mind-wandering were associated with cortical thinning in parietal and posterior temporal regions in the left hemisphere (which are important in the control of cognition and attention) as well as heightened connectivity between the intraparietal sulcus and a region that spanned limbic and default-mode regions in the ventral inferior frontal gyrus. Finally, we observed a dissociation in the thickness of the retrosplenial cortex/lingual gyrus, with higher reports of spontaneous mind-wandering being associated with thickening in the left hemisphere, and higher repots of deliberate mind-wandering with thinning in the right hemisphere. These results suggest that the intentionality of the mind-wandering state depends on integration between the control and default-mode networks, with more deliberation being associated with greater integration between these systems. We conclude that one reason why mind-wandering has a controversial relationship with control is because it depends on whether the thoughts emerge in a deliberate or spontaneous fashion.

Introduction

Conscious experience is not always tethered to the events taking place in the here and now: Indeed, in daily life, people's minds frequently wander away from the external environment toward inner musings (Kane et al., 2007, Killingsworth and Gilbert, 2010). One enduring puzzle concerning this common form of everyday thought is how it relates to cognitive control. Studies from multiple research groups have shown that people with low levels of control often experience relatively high rates of mind-wandering compared with people who have high levels of control (McVay and Kane, 2009, Mrazek et al., 2012; Unsworth and Mcmillan, 2013). However, this relationship is not consistently observed across task contexts. Indeed, research has shown that people with relatively high levels of control tend to engage in more mind-wandering during easy tasks than do people with relatively low control (e.g. Bernhardt et al., 2014; Levinson and Davidson, 2012; Rummel and Boywitt, 2014; Smallwood et al., 2013), presumably because (a) easy tasks afford people the opportunity to mind-wander without incurring performance costs, and (b) high-control individuals are better able to modulate their mind-wandering in accordance with task demands. Accordingly, it has been proposed that understanding the relationship between mind-wandering and control needs to take into account the ongoing task context as well as the nature of the mental content that occurs during the mind-wandering state (Smallwood and Andrews-Hanna, 2013, Smallwood and Schooler, 2015).

It has recently been suggested that one important aspect of mind-wandering is whether it is experienced as occurring deliberately or spontaneously (e.g. Seli et al., 2016b). Studies have found that individuals who report high levels of spontaneous mind-wandering in everyday life tend to score higher on measures of attention-deficit/hyperactivity disorder (ADHD; Seli et al., 2015b), obsessive-compulsive disorder (OCD; Seli et al., 2016a), and that they are more reactive to their inner experiences (Seli et al., 2015a). More recently, it has not only been shown that both types of mind-wandering are related to their corresponding state-levels when assessed in the laboratory (Seli et al., 2016c) – which indicates that the measures of spontaneous and deliberate mind-wandering have construct validity – but also that during easy tasks, deliberate mind-wandering is more frequently reported than is spontaneous mind-wandering (Seli et al., 2016b). The association between spontaneous mind-wandering and less controlled thought and behaviour, as well as the high incidence of deliberate mind-wandering during easy tasks, both raise the possibility that the difference between spontaneous and deliberate mind-wandering arises through differences in how these two mental experiences relate to cognitive control.

Confusion regarding how experiences such as mind-wandering relate to the control of cognition extends to the default-mode network (DMN), a neural system that has been suggested to be the basis of many features of the mind-wandering state (Fox et al., 2015, Gusnard and Raichle, 2001, Raichle et al., 2001). This large-scale network engages a constellation of regions including the medial prefrontal cortex, posterior cingulate cortex, regions of the angular gyrus, and anterior as well as medial aspects of the temporal lobe. Early interpretations of the functions of the DMN focused on its tendency to deactivate during demanding tasks (e.g. Raichle et al., 2001), as well as its anti-correlation with regions that are commonly activated during externally oriented tasks, such as the dorsolateral prefrontal cortex (Fox et al., 2005). These observations have led to conceptualizations of the role of the DMN in cognition as supporting automatic or self-relevant information processing (c.f. Anticevic et al., 2012; Hamilton et al., 2015). In addition, the DMN is generally contrasted with networks that are activated during demanding tasks, and which are important in the control of cognition, such as the fronto-parietal network (FPN; Cole et al., 2013; Duncan, 2010; Fedorenko et al., 2013).

It is often assumed that the DMN works in opposition to networks that support more controlled cognition (e.g. Anderson et al., 2016; Hellyer et al., 2014). However, recent studies have challenged this dichotomous view of DMN function, indicating that this network can play a role in active cognitive processing during demanding tasks. It is now thought that the DMN contributes to complex tasks by increasing connectivity with regions supporting cognitive control (e.g. Krieger-Redwood et al., 2016; Piccoli et al., 2015; Spreng et al., 2014, Spreng et al., 2010; Vatansever et al., 2015). These findings suggest that, despite evidence of an anti-correlation between the DMN and executive control systems at rest, there are functionally significant interactions between these systems that allow information from memory to make a contribution to a controlled train of thought. Critically, these findings support a hypothesised role for both of these systems when internal thought has a controlled or deliberate nature (see Smallwood et al. (2011) and Spreng (2012)). Given the evidence indicating that the DMN is active during mind-wandering (Allen et al., 2013, Christoff et al., 2009, Mason et al., 2007, Stawarczyk et al., 2011), it is possible that its interactions with systems such as the FPN may provide a mechanism through which experiences that occur during mind-wandering may be organised in a manner that is more closely aligned with a person's intentions (Fox et al., 2015, Seli et al., 2016d, Smallwood et al., 2012).

The current study used magnetic resonance imaging (MRI) to explore the hypothesis that the intentionality associated with the mind-wandering state depends on the brain's ability to integrate information from the DMN and the FPN. To do this, in a single session, we measured the structural and functional brain organisation of a large cohort of participants who had completed validated measures (Seli et al., 2016c) of spontaneous and deliberate mind-wandering (Carriere et al., 2013), which assess the rate at which people engage in these two types of mind-wandering in their daily lives. This design allowed us to test the neurocognitive architecture that underlies trait-level variation in the amount of deliberation in mind-wandering in two complementary ways. First, we performed a surface-wide cortical-thickness analysis to identify how variation in the grey-matter structure of the cortex relates to people's propensity to engage in deliberate and spontaneous mind-wandering. Second, we used seed-based functional connectivity to explore the function of sites with well-established roles in cognitive control: the inferior frontal sulcus, the intraparietal sulcus, and the pre-supplementary motor area, all of which are key nodes of the FPN (for a review see Duncan (2010)). We focused on regions in the frontal-parietal control system since, according to component-process accounts of the mind-wandering state (e.g. Smallwood, 2013, Smallwood and Schooler, 2015), these would provide the greatest chance to dissociate spontaneous and deliberate types of mind-wandering. If deliberate mind-wandering depends on the integration of the DMN and the FPN (Smallwood et al., 2011), then we expected to find that people who report more deliberate mind-wandering would have greater cortical thickness at the intersection of these two networks and greater functional integration between them. Based on the hypothesis that spontaneous mind-wandering may often result from problems in control, we expected that this form of mind-wandering would not be associated with greater cortical thickness in areas associated with cognitive control, or to be associated with as clear a pattern of coupling between the DMN and the FPN.

Section snippets

Participants

We analyzed data from 123 healthy volunteers (age: M=26.59, SD=4.23; 59 females) who were part of a larger cross-sectional data-collection study carried out at the Max Planck Institute (MPI) of Human Cognitive and Brain Sciences in Leipzig, Germany. Participants were recruited through advertisements and were screened for past and present psychiatric and neurological conditions before participation. All participants fulfilled the MRI safety requirements for the MPI and provided written informed

Cortical thickness

We first characterized the regions whose cortical thickness varied with the self-reported rates of deliberate and spontaneous mind-wandering (see Fig. 1). A cluster in the right prefrontal cortex (presented in green) had greater cortical thickness for participants who reported higher rates of deliberate mind-wandering. This extended from the dorsal regions of the medial prefrontal cortex to the inferior frontal sulcus. On the other hand, a cluster extending from the left intraparietal sulcus to

Discussion

In the current study, we sought to determine whether the integration between the DMN and executive network is related to inter-individual trait differences in rates of deliberate and spontaneous mind-wandering. Using a combination of different imaging modalities, we demonstrated that participants who reported higher rates of deliberate mind-wandering tended to show a pattern of heightened integration between the DMN and regions of the FPN. This pattern was observed primarily in prefrontal

Acknowledgements

EJ was supported by grants from BBSRC (BB/J006963/1) and the European Research Council (SEMBIND – 283530). FL was supported by the Swiss National Science Foundation (P2ZHP1_155200). JS was supported by the European Research Council (WANDERINGMINDS – 646927). JS and DSM received support from the Volkswagen Foundation (Wandering Minds – 89440 and 89439). This publication was also made possible through the support of a grant from the John Templeton Foundation, “Prospective Psychology Stage 2: A

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