Elsevier

Brain and Cognition

Volume 132, June 2019, Pages 118-128
Brain and Cognition

Patterns of on-task thought in older age are associated with changes in functional connectivity between temporal and prefrontal regions

https://doi.org/10.1016/j.bandc.2019.04.002Get rights and content

Highlights

  • Connectivity between the left ATL and prefrontal cortex decreases in ageing.

  • Lower brain connectivity in young adults is linked to flexibility in ongoing thought.

  • Lower brain connectivity in older adults is linked to preserved creative performance.

  • Deliberate on-task thoughts and visual thoughts are increased in ageing.

Abstract

Humans spend a large proportion of their time engaged in thoughts unrelated to the task being performed, a tendency that declines with age. However, a clear neuro-cognitive account of what underlies this decrease is lacking. This study addresses the possibility that age-related changes in off-task thinking are correlated with changes in the intrinsic organisation of the brain. Laboratory measures of ongoing thought were recorded in young and older individuals, who also participated in a resting state fMRI experiment. Older individuals showed reduced connectivity between the left anterior temporal lobe with prefrontal aspects of the DMN. We found that off-task thinking did not increase when task demands were lower for older adults, which is a pattern repeatedly seen in younger individuals. Finally, we demonstrated that these neural and thought patterns were linked – for younger participants only, reductions in the strength of connectivity were related to a greater shift towards off-task thoughts when task demands decreased. Importantly, in the older individuals, lower connectivity between the same regions was linked to preserved performance on a creativity task. These data suggest that the age-related reduction of off-task thought may be related to reduced communication between temporal and prefrontal DMN regions in ageing.

Introduction

The ability to self-generate thoughts in imagination is a central aspect of human cognition. Between a third to half of our waking life is spent engaged in experiences that are unrelated to events in the here and now (Kane et al., 2007). Given their ubiquity, it is hardly surprising that self-generated thoughts are linked to useful features of human cognition including: planning (Baird, Smallwood, & Schooler, 2011), temporal decision making (Smallwood, Ruby, & Singer, 2013), memory (Poerio et al., 2017) and creative problem solving (Baird et al., 2012, Leszczynski et al., 2017, Smeekens and Kane, 2016, Wang et al., 2018). States or patterns of off-task thought have also been linked to lapses in performance during working memory tasks (McVay and Kane, 2009, Mrazek et al., 2012), an association that is argued to emerge partly because attention is directed away from events in the immediate environment (a phenomenon known as ‘decoupling’; Smallwood, 2013). Hence, it is argued that self-generated thoughts can be beneficial in everyday life, despite costs on task performance, especially if they occur in a context in which deficits in performance are unlikely (Smallwood & Andrews-Hanna, 2013). One well documented and robust characteristic of off-task thought is its reduction with increasing age (Giambra, 1989, Jackson and Balota, 2012, Jackson et al., 2013, McVay et al., 2013, Martinon et al., in press). Although the association between ageing and reduced off-task thought is well documented in the literature, we currently lack a clear neuro-cognitive account of this age-related decline.

Component process accounts of off-task thought emphasise the dual importance of processes involved in: (1) the production of mental content that is not related to the external environment, and (2) the control processes that are important for the regulation of these experiences (Christoff, Irving, Fox, Spreng & Andrews-Hanna, 2016; Smallwood, 2013, Smallwood and Schooler, 2015). Broadly, these accounts propose that the generation and representation of off-task thoughts are subserved by memory representation processes whereas the control of off-task thought occurrence is subserved by executive control processes (McVay and Kane, 2009, Smallwood and Andrews-Hanna, 2013). From a theoretical perspective, age-related declines in off-task thought may emerge from declines in the integrity of neurocognitive processes either related to memory, control, or both. To investigate these possibilities, our study combines laboratory measures of ongoing thought patterns in young and older individuals, with measures of intrinsic neural organisation provided by resting state functional magnetic resonance imaging. In our study we aimed to characterise the underlying neural changes linked to ageing and examine whether these are associated with age-related changes in patterns of ongoing thought. While the literature often focuses on the relationship between off-task thought and ageing, we explored the effects of age on a range of aspects of ongoing thought using Multi-Dimensional Experience Sampling (MDES). In this way we hoped to provide valuable information with regards to the potential neural correlates of age-related changes in patterns of ongoing thought.

According to contemporary theory, memory processes provide representational information upon which the content of self-generated experiences are based (Baird et al., 2011; **Christoff et al., 2016, Poerio et al., 2017, Tulving, 2002), and it is well known that changes in conceptual and episodic knowledge occur with age (Addis et al., 2010, Addis et al., 2008, Schmitter-Edgecombe et al., 2000). Evidence from cognitive neuroscience suggests memory processes are linked to temporal lobe structures, including both anterior regions of the lateral temporal cortex, and regions on the medial surface such as the hippocampus (Davey et al., 2016, Ellamil et al., 2016, Ralph et al., 2017). At rest, these regions show increased functional connectivity with medial and lateral regions in the posterior and anterior cortical regions, and collectively form what is known as the Default Mode Network (DMN) (Andrews-Hanna, 2012, Buckner et al., 2008, Raichle, 2015, Spreng et al., 2008). In older age, reduction of both activity and connectivity of the DMN have been reported (Biswal et al., 2010, Damoiseaux et al., 2008, Damoiseaux, 2017). Regions closely allied to the core DMN also change with age, including regions of temporal cortex (Fjell et al., 2009, Raz et al., 2004) and hippocampus (Allen et al., 2005, Du et al., 2006, Raz et al., 2010). In healthy young adults, connectivity of the hippocampus is related to changes in spatial, episodic and semantic memory (Persson et al., 2018, Sormaz et al., 2017) and age-related changes in this domain can mediate cognitive abilities such as episodic memory (Fjell & Walhovd, 2010).

As well as processes important for generating off-task experience, contemporary accounts emphasise the need to understand how they are regulated (Andrews-Hanna et al., 2014, McVay and Kane, 2010). It is generally assumed that the regulation of task-unrelated states depends in part upon executive control processes (Kane and McVay, 2012, Levinson et al., 2012, Rummel and Boywitt, 2014). As such, individuals with high working memory capacity (Rummel & Boywitt, 2014), who make patient economic choices (Smallwood et al., 2013), or who score high on measures of intelligence (Turnbull et al., 2019) flexibly adjust their off-task experience to demands of the environment. Neural studies suggest that important aspects of executive control are linked to processes in regions of lateral frontal and parietal cortex that show elevated activity across a wide range of task domains (Duncan and Owen, 2000, Fedorenko et al., 2013). In younger adults, the connectivity between regions important for executive control predicts working memory performance and intelligence (Finn et al., 2015), cognitive features highly related to off-task thoughts (Kane and McVay, 2012, Mrazek et al., 2012). Critically, older adults display altered connectivity patterns between frontal and parietal areas (Meunier et al., 2009, Wu et al., 2012), as well as poorer working memory capacity (Braver & West, 2008), suggesting off-task thoughts regulation may prove difficult in ageing.

Accumulating evidence in younger adults supports a role of both the default mode and frontoparietal networks in off-task states. Experience sampling studies, in conjunction with fMRI, have shown that both networks are active during periods of off-task thought (Allen et al., 2013, Christoff et al., 2009, Stawarczyk et al., 2011). Studies have also examined individual variation in off-task experience and how they relate to the organisation of neural functioning. Smallwood et al. (2016) found that variation in regions of both the temporal pole and the hippocampus were related to variations in ongoing experience patterns including episodic quality, detail, and relationship to an ongoing task. Regions of the frontal-parietal cortex are also important in the off-task state: studies suggest that the connectivity of the DMN and frontoparietal network is stronger for individuals who spend more time off-task (Mooneyham et al., 2016), especially when off-task thinking is deliberate (Golchert et al., 2017).

In our study, we used a combination of experience sampling and resting state fMRI to explore whether age-related neural changes are associated with changes in patterns of ongoing thought. To this aim, young and older participants performed a working memory task with varying difficulty, during which patterns of thoughts were measured using a set number of questions targeting thought content, this method is referred as Multi-Dimensional Experience Sampling (MDES). For a complete consideration of the cognitive functions relating to ongoing experiences, measures of fluid intelligence, creativity and working memory were taken. Participants also underwent a resting state functional connectivity scan allowing us to describe each individual in terms of their intrinsic architecture at rest. For our connectivity analyses three sets of seed regions targeting different theories for the age-related decrease of off-task thoughts were selected. To consider the implications of systems important for mental representation, seed regions from the temporal lobe linked to memory were used: the left and right hippocampus and left and right anterior temporal lobe (Patterson, Nestor & Rogers, 2007; Tulving, 2002). We also selected regions in the left and right pre-frontal cortex which are linked to processes of cognitive control within the memory domain. Specifically, we selected the left and right inferior frontal gyrus to explore the involvement of systems important for semantic control (Noonan, Jefferies, Visser, & Lambon Ralph, 2013).

Section snippets

Participants

The older adults’ group was composed of 22 women and 17 men (Mage = 66.08 years, range = 55–87) recruited using opportunity sampling. The younger adult group consisted of 32 women and 9 men (Mage = 19.73 years, range = 18–23) who were undergraduate students in psychology at the University of York. All participants were remunerated for their time and travel. Participants were required to be native English speakers, right-handed, and to have a normal or corrected vision and hearing. Exclusion

Behavioural performance

We examined differences in performance according to age (young vs. older) for relevant behavioural measures. These comparisons used a Multivariate Analysis of Variance (MANOVA) and revealed group differences for all measures except the Unusual Uses Test (Digit symbol substitution test, F (1, 65) = 29.54, p < .001, ηp2 = 0.31; National Adult Reading Test, F (1, 65) = 54.75, p < .001, ηp2 = 0.46, Ravens Progressive Matrices, F (1, 65) = 35.38, p < .001, ηp2 = 0.35, Unusual Uses Test, F (1,

Discussion

Our study set out to understand whether different patterns of ongoing thought in older individuals could be linked to age-related changes in the underlying functional architecture. We selected three regions, each linked to different processes based on prior research: the hippocampus given its role in episodic memory, the anterior temporal lobe given their role in semantic memory and the inferior frontal gyrus given its role in control of memory in both domains (Stampacchia et al., 2018). Our

Declaration of interests

The authors declared that there is no conflict of interest.

Acknowledgments

This project was supported by European Research Council Consolidator awarded to JS (WANDERINGMINDS – 646927) and an award from The Dunhill Medical Trust to JS, LMR and EJ [R422/0515].

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