Elsevier

NeuroImage

Volume 98, September 2014, Pages 359-365
NeuroImage

Anticipatory processes in brain state switching — Evidence from a novel cued-switching task implicating default mode and salience networks

https://doi.org/10.1016/j.neuroimage.2014.05.010Get rights and content

Highlights

  • A cued-switching task was used to study anticipatory processes in state switching.

  • Briefly presented rest-cues elicited activation in the DMN.

  • Between-state (rest-to-task) switch cues elicited anticipatory DMN attenuation.

  • Task-to-rest cues yielded DMN up-regulation.

  • The core hub of the SN–rAI is the most responsive to switches from rest.

Abstract

The default mode network (DMN) is the core brain system supporting internally oriented cognition. The ability to attenuate the DMN when switching to externally oriented processing is a prerequisite for effective performance and adaptive self-regulation. Right anterior insula (rAI), a core hub of the salience network (SN), has been proposed to control the switching from DMN to task-relevant brain networks. Little is currently known about the extent of anticipatory processes subserved by DMN and SN during switching. We investigated anticipatory DMN and SN modulation using a novel cued-switching task of between-state (rest-to-task/task-to-rest) and within-state (task-to-task) transitions. Twenty healthy adults performed the task implemented in an event-related functional magnetic resonance imaging (fMRI) design. Increases in activity were observed in the DMN regions in response to cues signalling upcoming rest. DMN attenuation was observed for rest-to-task switch cues. Obversely, DMN was up-regulated by task-to-rest cues. The strongest rAI response was observed to rest-to-task switch cues. Task-to-task switch cues elicited smaller rAI activation, whereas no significant rAI activation occurred for task-to-rest switches. Our data provide the first evidence that DMN modulation occurs rapidly and can be elicited by short duration cues signalling rest- and task-related state switches. The role of rAI appears to be limited to certain switch types — those implicating transition from a resting state and to tasks involving active cognitive engagement.

Introduction

The brain at rest is characterized by coherent spontaneous low-frequency fluctuations across multiple discrete brain networks (i.e. resting state networks; RSNs) (Damoiseaux et al., 2006, De Luca et al., 2005). The default mode network (DMN) (Raichle et al., 2001) incorporates frontal and posterior midline regions, including medial prefrontal cortex (mPFC), and posterior cingulate cortex (PCC)/precuneus. This neural circuit controls internally-oriented, self-referential cognition (Buckner et al., 2008, Gerlach et al., 2011, Spreng and Grady, 2010). DMN activity increases during wakeful rest, and tasks of self-referential, introspective cognition, but is attenuated following the switch to externally-oriented attention-demanding tasks (Spreng and Grady, 2010, Spreng et al., 2010). Increase in cognitive load across a range of cognitive tasks, generally those, that do not involve social and/or self-referential processing, leads to enhanced DMN suppression (McKiernan et al., 2003, Pyka et al., 2009, Singh and Fawcett, 2008). Moreover, processing efficiency during those tasks is correlated with the degree of DMN attenuation (Greicius et al., 2003, Greicius and Menon, 2004, Meyer et al., 2012). According to the DMN interference hypothesis (Sonuga-Barke and Castellanos, 2007), insufficient DMN suppression during the switch to externally-oriented cognitively-demanding tasks interferes with task performance, producing periodic lapses of attention (Bendarski et al., 2011, Li et al., 2007, Weissman et al., 2006), and increased intra-individual behavioural variability (Sandrone and Bacigaluppi, 2012).

Comparatively little is known about the process, in contrast to the outcome, of these switches between resting and task related states. Initial research highlights the importance of preparatory processes occurring just prior to active task engagement controlling DMN attenuation. Sridharan et al. (2008) observed increased activation in right fronto-insular cortex (rFIC), (which together with anterior cingulate cortex (ACC) is part of the salience network [SN]), prior to both DMN attenuation and increased activation in neural circuits supporting task-specific processing. This led Menon and Uddin (2010) to propose the hypothesis that right anterior insula (rAI), is a critical hub initiating switches between DMN and brain networks of goal-directed, task-specific engagement. In addition, Bonnelle et al. (2012) have shown that effective DMN modulation depends on the structural integrity of SN.

The classical cognitive control experiments investigating preparatory processes during switching between tasks have shown a robust involvement of the fronto-parietal network in task set initiation (Monsell, 2003) along with anticipatory pre-activation of specific brain areas relevant for the execution of a particular upcoming task (Wylie et al., 2006). Such studies typically employ cued task-switching paradigms, consisting of a series of discrete trials on which participants perform one of a limited number of different tasks, i.e., on some trials they are prompted to repeat the immediately preceding task (non-switch trials), on others they are asked to perform a different task (switch trials) (Kiesel et al., 2010, Wylie et al., 2006). The use of anticipatory cueing in such paradigms enables the investigation of the preparatory cognitive and neural processes occurring before the actual initiation of goal-directed actions (Brass and von Cramon, 2002, Meiran et al., 2010). Although the role of the SN, specifically rAI, has generally not been the central focus of investigation in these studies, robust responses of both ACC and rAI have been commonly reported (Dove et al., 2000). Thus, the widespread functions of rAI suggest this region to be a general multimodal integration unit, which operates by gathering motivationally salient information, facilitating the appropriate neural reconfiguration and higher-level cognitive processing (Cauda et al., 2012, Chang et al., 2013, Downar et al., 2000, Downar et al., 2001, Downar et al., 2002, Kurth et al., 2010, Uddin et al., 2014). In turn, this highly coordinated processing is essential for effective cognitive control during different types of cognitive or mental switches.

Here we investigate the switch-related anticipatory processes with a task that extends the classical cued task-switching paradigm to also study state-to-state switches, i.e. switches from rest-to-task and vice versa. Crucially, this novel design enables the identification and comparison of the neural reconfiguration and associated network activations during the anticipation of both within- (task-to-task) and between-state switches.

The current study addresses three questions. First, from a methodological point of view we need to establish that our newly developed task provides a valid way of studying DMN attenuation during state-to-state switch anticipation. Thus, the first question is — is the DMN, shown previously to be implicated in steady-state rest, responsive to cues signalling rest? If so, is this DMN activity attenuated to cues of an upcoming task? Second, previous studies have only focused on DMN suppression following the switch from rest-to-task; here we raise the related question concerning the anticipation of switches in the opposite direction, i.e., is there an up-regulation of DMN following the presentation of cues signalling an upcoming switch from task-to-rest? Finally, we examine the role of rAI during the anticipation of different switch types. Thus, the third question is — is rAI equally involved in within- and between-state switch anticipation?

To address these questions we developed a new paradigm and implemented it within an event-related experimental design in which visual cues signalled the nature of the following trial while fMRI was being acquired. We included rest trials and two different types of task trials. With regard to our three research questions we predicted that: (i) DMN will be activated in response to rest cues and that this activity will be attenuated by rest-to-task switch cues; (ii) cues signalling the switch from task-to-rest will elicit anticipatory DMN up-regulation; and (iii) in keeping with the model of Menon and Uddin (2010), state-to-state switches requiring DMN disengagement will elicit the highest rAI response.

Section snippets

Participants

Twenty healthy adults with no prior history of neurological or psychiatric disease participated in the study. They all had an IQ in the average and above average range IQ (> 85) measured by the Ward 7-subtest short form of the Wechsler Adult Intelligence Scale-III (Pilgrim et al., 1999), mean IQ = 117.9 (SD = 11.2). Study participants were recruited via internet, magazine and internal university advertising. Two subjects had to be excluded from further analysis due to excessive head motion. The

Results

Participants performed with a very high degree of accuracy (correct responses > 98% (SD = 1.28). A GLM repeated measures analysis of variance (ANOVA) revealed a main effect of switch type (F (2, 34) = 21.78, p < .001). A task switching (task-to-task) cost was observed with slower response times (RT) on task switch than non-switch trials. The rest-to-task switch cost was smaller but still statistically significant (task-to-task switch: 873 ms, p < .001; rest-to-task switch: 809 ms, p = .007; task repeat: 738 

Discussion

The current study provides the first evidence of the rapid modulation of DMN and SN during state-to-state transitions using a cued-switching task.

Acknowledgments

We thank Ruth Seurinck and Wouter De Baene for their help with the experimental design, data acquisition and insightful comments on data analysis. This work is supported by the Fund for Scientific Research — Flanders (project number: 3G084810).

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