Shaped by our thoughts – A new task to assess spontaneous cognition and its associated neural correlates in the default network
Introduction
Spontaneous, self-generative thought – or mind wandering – has been a topic of burgeoning interest for cognitive neuroscientists in recent years. Converging evidence suggests we spend upwards of half of our waking day engaged in mind wandering (Killingsworth & Gilbert, 2010) and that such internal mentation can confer important benefits on our emotional well-being and our ability to engage in forward planning, decision making, self-reflection and social–emotional processing (Immordino-Yang et al., 2012, Laird et al., 2009, McMillan et al., 2013, Smallwood and Andrews-Hanna, 2013, Uddin et al., 2007).
In task-based assessment, mind wandering has been associated with activity in a distributed set of brain regions known as the default network (DN) (Christoff et al., 2009, Mason et al., 2007, Stawarczyk et al., 2011b). This anatomically defined brain system comprises regions in the prefrontal, temporal, and parietal cortices, which converge on core midline hubs in the posterior cingulate and anteromedial prefrontal cortex (Andrews-Hanna, 2012). Although the precise functions of the DN remain a matter of debate, mounting evidence points to two distinct DN subsystems that may mediate dissociable aspects of internal mentation, namely, memory-based construction/simulation (medial temporal lobe/MTL subsystem) and introspection about mental states (dorsal medial prefrontal cortex/dmPFC subsystem) (Andrews-Hanna et al., 2014, Buckner et al., 2008). Stronger resting state functional connectivity within the DN has been associated with higher frequencies of spontaneous thought and engagement in mind wandering (Andrews-Hanna et al., 2010a, Wang et al., 2009, Yang et al., 2013). Nevertheless, regions outside the DN have also been implicated in mind wandering, in particular executive control systems (Christoff et al., 2009), yet the exact role these systems play in mind wandering remain to be elucidated (Franklin et al., 2013, McVay and Kane, 2010, Smallwood, 2013).
Given the spontaneous emergence of mind wandering and its internally directed nature, it is a complex phenomenon to assess in an experimental setting. The most common approaches to mind wandering assessment involve participants performing a concurrent attention-demanding task, such as the Sustained Attention to Response Task or text reading, often requiring them to self-identify when “off-task” thoughts occur. Qualitative aspects of mind wandering have been explored, whereby participants may also be trained to classify the “off-task” thoughts – or this is done by the experimenter – into broad categories that reflect the temporal orientation of the thought (Smallwood, Nind, & O’Connor, 2009), the degree of stimulus/task-relatedness (Stawarczyk, Majerus, Maj, Van der Linden, & D’Argembeau, 2011a) or whether it was a form of autobiographical planning (Baird, Smallwood, & Schooler, 2011). Notably, however, this assessment of phenomenological content has been mostly limited to these broad categorisation methods, with limited attempts to map potentially dissociable forms of internal mentation onto established DN subsystems.
While significant advances have been made in the use of cognitive tasks to explore the structure and function of the DN (Andrews-Hanna et al., 2014), a number of issues remain unresolved. Crucially, the extent to which a concurrent task demands attention, and the meta-awareness required to self-identify and self-classify thoughts, restricts its broader application to clinical populations with reduced cognitive resources. Evidence suggests that in the context of low task-demands subjects report more off-task thoughts, compared to reports during more demanding tasks (McVay, Meier, Touron, & Kane, 2013). This highlights that assessment using tasks with low cognitive demands may be more likely to elicit instances of mind wandering. At present, there is a lack of available paradigms to investigate mind wandering in a context free from additional loadings on attention and working memory processes. This renders mind wandering assessment particularly difficult in neurodegenerative diseases or psychiatric conditions, where the integrity of the default network is compromised significantly and progressively, from early in the disease course (Broyd et al., 2009, Damoiseaux et al., 2012, Hafkemeijer et al., 2012, Seeley et al., 2009, Whitfield-Gabrieli and Ford, 2012). Developing measures of spontaneous cognition suitable for these populations is critical, in order to establish the functional outcomes of damage to the DN.
To address this gap in the literature we developed a novel thought sampling task designed for the assessment of mind wandering in clinical syndromes, as it is free from the cognitive demands imposed by performing a concurrent task, and from requirements of self-identification and self-classification of thoughts. For the first time, we present a scoring system developed to assess both the frequency of mind wandering, and its qualitative content with respect to potentially dissociable styles of self-generative thought based on a functional–anatomical fractionation of the DN (Andrews-Hanna, 2012). Here, we present behavioural data from a sample of healthy older controls. We specifically chose to validate the task in a cohort that is age-matched to clinical samples in which DN pathology typically manifests (e.g., (Buckner et al., 2008)), with a view to applying the validated task in dementia populations in subsequent studies. We further present resting state functional connectivity imaging analyses to demonstrate that performance on this novel task maps onto specific patterns of functional connectivity in the DN. To our knowledge, this study represents the first attempt to develop a task designed specifically to explore both the frequency and phenomenological content of mind wandering episodes, in the context of minimal cognitive demands.
Section snippets
Participants
Thirty-one healthy older participants (age range: 53–79, with an average age of 66.9 years and average education of 14.9 years) were recruited from two volunteer research panels and screened for cognitive dysfunction using global assessment scales (the Mini-Mental Status Examination; MMSE (Folstein, Folstein, & McHugh, 1975) and the Montreal Cognitive Assessment; MoCA (Nasreddine et al., 2005)). Participants were deemed suitable for inclusion in the study if they scored above a cut-off score of
Overall mind wandering frequency
Fig. 2 displays the proportion of responses across each of the four levels on the Shape Expectations task, for the overall participant sample. Comparison via t-test revealed that there was no difference in the proportion of responses per level (1–4) between the overall sample and the imaging subset (all p values > .9). In the repeated measures ANOVA, as Mauchly’s Test of Sphericity indicated that the assumption of sphericity had been violated (χ2(5) = 14.49, p < .05), the Greenhouse–Geisser
Discussion
We present data from a novel thought sampling task that effectively probes the frequency and qualitative content of mind wandering during conditions of low cognitive demand. Using resting state correlational analysis, we confirmed that mind wandering on the experimental task was significantly associated with specific patterns of functional connectivity in the DN. To our knowledge, this experimental paradigm represents the first measure to provide an “online” assessment of mind wandering in the
Conflict of interest
The authors declare no competing financial interests.
Acknowledgments
CO is supported by an Alzheimer’s Australia Dementia Research Foundation PhD scholarship. JMS has no financial disclosures to make. SJGL is supported by a National Health and Medical Research Council Practitioner Fellowship (1003007). JRAH is supported by a National Institutes of Mental Health Fellowship (5F32MH093985). MI is supported by an Australian Research Council Discovery Early Career Research Award (DE130100463). The authors would also like to thank the three anonymous Reviewers for
References (69)
- et al.
Age-related neural changes in autobiographical remembering and imagining
Neuropsychologia
(2011) - et al.
Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration
Neuropsychologia
(2007) - et al.
Functional-Anatomic Fractionation of the Brain’s Default Network
Neuron
(2010) - et al.
The role of default network deactivation in cognition and disease
Trends in Cognitive Sciences
(2012) - et al.
Back to the future: Autobiographical planning and the functionality of mind-wandering
Consciousness and Cognition
(2011) - et al.
Default-mode brain dysfunction in mental disorders: A systematic review
Neuroscience and Biobehavioral Reviews
(2009) - et al.
Mini-Mental State: A practical method for grading the cognitive state of patients for the clinician
Journal of Psychiatric Research
(1975) - et al.
Imaging the default mode network in aging and dementia
Biochimica et Biophysica Acta (BBA) – Molecular Basis of Disease
(2012) - et al.
Episodic future thinking is impaired in the behavioural variant of frontotemporal dementia
Cortex
(2013) - et al.
Dynamic functional connectivity of the default mode network tracks daydreaming
NeuroImage
(2014)
Linking DMN connectivity to episodic memory capacity: What can we learn from patients with medial temporal lobe damage?
NeuroImage: Clinical
Flexible modulation of network connectivity related to cognition in Alzheimer’s disease
NeuroImage
Aging ebbs the flow of thought: Adult age differences in mind wandering, executive control, and self-evaluation
Acta Psychologica
Meta-awareness, perceptual decoupling and the wandering mind
Trends in Cognitive Sciences
Neurodegenerative diseases target large-scale human brain networks
Neuron
Tricks of the mind: Visual hallucinations as disorders of attention
Progress in Neurobiology
Cooperation between the default mode network and the frontal–parietal network in the production of an internal train of thought
Brain Research
Segmenting the stream of consciousness: The psychological correlates of temporal structures in the time series data of a continuous performance task
Brain and Cognition
When is your head at? An exploration of the factors associated with the temporal focus of the wandering mind
Consciousness and Cognition
Mind-wandering: Phenomenology and function as assessed with a novel experience sampling method
Acta Psychologica
The self and social cognition: The role of cortical midline structures and mirror neurons
Trends in Cognitive Sciences
Exploring the brain network: A review on resting-state fMRI functional connectivity
European Neuropsychopharmacology
When the mind wanders: Age-related differences between young and older adults
Acta Psychologica
The brain’s default network and its adaptive role in internal mentation
The Neuroscientist
Evidence for the default network’s role in spontaneous cognition
Journal of Neurophysiology
The default network and self-generated thought: Component processes, dynamic control, and clinical relevance
Annals of the New York Academy of Sciences
Medial and lateral networks in anterior prefrontal cortex support metacognitive ability for memory and perception
The Journal of Neuroscience
What about the “self” is processed in the posterior cingulate cortex?
Frontiers in Human Neuroscience
The brain’s default network
Annals of the New York Academy of Sciences
Age differences in the intrinsic functional connectivity of default network subsystems
Frontiers in Aging Neuroscience
The precuneus: A review of its functional anatomy and behavioural correlates
Brain
Experience sampling during fMRI reveals default network and executive system contributions to mind wandering
Proceedings of the National Academy of Sciences
Functional connectivity tracks clinical deterioration in Alzheimer’s disease
Neurobiology of Aging
Brains creating stories of selves: The neural basis of autobiographical reasoning
Social Cognitive and Affective Neuroscience
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2020, Consciousness and CognitionCitation Excerpt :We then went beyond previous work to examine the effect of this manipulation on a range of features of spontaneous thoughts, including their temporal orientation, verbal or visual form, perspective, goal orientation, social orientation, whether they were real or fantasy-based, temporal distance, level of detail, and vividness of imagery. We incorporated aspects of Miles, Karpinska, et al.’s (2010) methodology within a novel paradigm designed to free participants from the demands imposed by performing vigilance tasks and the requirement to self-identify MW thoughts (O’Callaghan, Shine, Lewis, Andrews-Hanna, & Irish, 2015; Seno, Ito, & Sunaga, 2011; Smallwood & Schooler, 2015). We believed this novel approach would induce high levels of MW and, combined with a triangulation of ES methods (namely probe-caught, retrospective, and open-ended), would enable us to collect comprehensive information about MW experiences.
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