Overcoming residual interference in mental set switching: Neural correlates and developmental trajectory

Abstract

Mental set switching is a key facet of executive control measured behaviorally through reaction time or accuracy (i.e., ‘switch costs’) when shifting among task types. One of several experimentally dissociable influences on switch costs is ‘task set inertia’, conceptualized as the residual interference conferred when a previous stimulus–response tendency interferes with subsequent stimulus processing on a new task. Task set inertia is thought to represent the passive decay of the previous stimulus–response set from working memory, and its effects decrease with increased interstimulus interval. Closely spaced trials confer high task set inertia, while sparsely spaced trials confer low task set inertia. This functional magnetic resonance imaging (fMRI) study characterized, for the first time, two opposing brain systems engaged to resolve task set inertia: 1) a frontoparietal ‘cortical control’ network for overcoming high task set inertia interference and 2) a subcortical-motor network more active during trials with low task set inertia. These networks were distinct from brain regions showing general switching effects (i.e., switch > non-switch) and from other previously characterized interference effects. Moreover, there were ongoing maturational effects throughout adolescence for the brain regions engaged to overcome high task set inertia not seen for generalized switching effects. These novel findings represent a new avenue of exploration of cognitive set switching neural function.

Introduction

A key facet of executive control is the capacity to rapidly, flexibly, and effectively switch mental sets among different types of information in a quickly changing environment, commonly referred to as ‘set switching’ (also termed ‘set shifting’, ‘task switching’, ‘attention switching’, ‘task-shifting’, or ‘attention shifting’) (Corbetta et al., 1993, Huston et al., 1937, Jersild, 1927, Smith et al., 2001, Wager et al., 2004). Despite the numerous and often conflated terms used to describe this cognitive process, it is generally assumed that the act of switching is subserved by a set of executive control parameters necessary to complete the task, termed a ‘task set’ (Logan and Gordon, 2001, Rogers and Monsell, 1995). Behaviorally, the presence of executive control needed to effect a mental set switch can be quantified in terms of ‘switch costs.’ Switch costs are typically defined as loss of accuracy or response speed when one task is interrupted in order to switch to another. Several behavioral studies have shown that switch costs involve multiple, experimentally dissociable influences (Allport et al., 1994, Meiran, 1996, Rogers and Monsell, 1995). Logan and Gordon (2001) theorized that switch costs measure the time it takes to implement new executive control parameters in a ‘task set’. Others have proposed a proactive component of control that partially reconfigures cognitive resources when impending set switches are prompted by an external cue, termed task set reconfiguration (Meiran, 1996, Meiran, 2000, Rogers and Monsell, 1995). Although such cue-guided mental preparation greatly reduces switch costs, it does not eliminate them (Cepeda et al., 2001, Meiran, 1996). The presence of residual behavioral costs implies that there is at least one other important cognitive factor at play in mediating switches of mental set. Another component has been conceptualized as ‘task set inertia’ (Allport et al., 1994, Meiran, 1996). Task set inertia is believed to represent the degree of residual interference conferred when a previous stimulus–response tendency interferes with the next stimulus (Rogers and Monsell, 1995). Unlike task set reconfiguration, task set inertia is thought to be passive and to decrease with time as the previous task set decays from working memory (Allport et al., 1994). Initially proposed to last several minutes (Allport et al., 1994), subsequent studies have shown that task set inertia resolves immediately following a switch during ongoing performance (Rogers and Monsell, 1995). Experimentally, the influence of task set inertia on switch costs can be seen by altering the interval between trials, with shorter intervals corresponding to greater degree of residual interference to overcome and producing greater behavioral switch costs.

The behavioral independence of task set inertia from other influences on switch costs (Rogers and Monsell, 1995) suggests that overcoming this residual interference could require distinct neural resources, perhaps similar to those engaged to overcome either stimulus–response compatibility interference or Stroop interference (Nee et al., 2007). The neural correlates of mental set switching have been fairly well described in two separate meta-analyses of 31 (Wager et al., 2004) and 18 (Buchsbaum et al., 2005) fMRI and PET studies. These meta-analyses have linked set switching to numerous cortical regions, including the caudal anterior cingulate cortex, premotor cortex, bilateral inferior parietal sulci, and right dorsolateral prefrontal cortex, as well as bilateral insula, and bilateral thalamus. Although many of these regions have been individually linked to other executive abilities such as working memory and response inhibition (Wager and Smith, 2003, Wager et al., 2004), there is evidence that these brain regions taken together are reliably and specifically engaged more during switch trials than during non-switch trials across several types of set switching tasks (Wager and Smith, 2003). Such an overlap between switching and other cognitive processes should not be wholly unexpected as switching is thought to rely on the integrity of several cognitive systems, including attention, inhibition, and working memory (Miyake et al., 2000). Several studies have also suggested that the basal ganglia play a role in set switching (Casey et al., 2002, Casey et al., 2004, Luna et al., 2001, Sohn et al., 2000). However, because basal ganglia engagement has not been consistently supported by set switching neuroimaging studies, it has been proposed that frontostriatal, or perhaps other prefrontal-subcortical, engagement in set switching is required only when the experimental paradigm requires the inhibition of certain competing cognitive or motor responses (Cools, 1980, Mink, 1996). Alternatively, the purpose of subcortical brain activation in this context might instead be to help maintain or switch between competing behavioral sets, as has been previously proposed (Alexander and Crutcher, 1990). Within the mental set switching literature, however, there is no consensus as to a definitive role for the basal ganglia in the underlying cognitive processes.

In sum, although previous behavioral and functional neuroimaging studies have firmly established the existence of residual task set inertia switch costs, their neural correlates and functional interpretation remain to be determined. No previous investigators have sought to characterize the neural correlates of task set inertia as distinct from set switching in general, despite the likelihood of its unique and important contribution to cognitive control. At least one study has indirectly examined possible task set inertia effects. Although it was not the primary aim of the study, Loose et al. (2006) contrasted fMRI-measured brain activity to switch trials preceded by a short (850 ms) versus a longer interval (1600 ms). They reported greater bilateral dorsolateral prefrontal activation to shorter intervals, interpreted as greater top-down control (Loose et al., 2006). However, this study was limited by a small sample size, by an inability to fully dissociate brain activity to different types of events due to its block design, and by not holding task set reconfiguration demands constant to ensure the neural results were specific to overcoming task set inertia. The vast majority of other published neuroimaging studies have examined set switching by contrasting switch and non-switch trials on average, which does little to differentiate the separate contributions of different cognitive processes and brain functions to switch costs.

Several studies have shown mental set switching task performance reaches near-adult levels around age 12, with non-significant switch cost decreases between adolescence and adulthood thereafter (Anderson, 2002, Casey et al., 2004, Davidson et al., 2006, Rubia et al., 2006, Waber et al., 2007). A recent behavioral study (Crone et al., 2006a) found switch costs decreased both with increasing interstimulus interval length and age, indicating that children and early adolescents have more difficulty than adults performing mental set shifts in the presence of high task set inertia. Two previous fMRI developmental set switching studies found numerous brain regions exhibiting positive and negative age-related activity changes (Casey et al., 2004, Rubia et al., 2006), suggesting a progressive development in task-specific frontoparietal and striatal regions related to an increased capacity of cognitive control functions. This indicates that although near-adult levels of set switching behavioral performance are achieved by adolescence, there remain important maturational changes in set switching related neural activity until adulthood. No study has yet examined task set inertia development specifically, so it is unclear how similar developmental changes may be instantiated in TSI-related brain activity levels. As with set switching, it is likely that relatively mature networks engaged to overcome task set inertia are already in place by puberty, but that these networks are differentially activated throughout adolescent development as cortical connections and long-distance white matter pathways are refined (Spencer-Smith and Anderson, 2009, Thatcher, 1992, Thatcher, 1997). Such developmental changes might be observed as changes in amplitude of regional brain activity or changes in the overall distributed profile of activation. Current neurodevelopmental theories propose that maturation of some executive functions is accompanied by changes from diffuse activation patterns to more localized patterns (Casey et al., 2005), characterized by greater activation of key task-specialized brain regions and decreased activity in superfluous regions (e.g., subcortical regions). In parallel, it has also been suggested that the functional network organization of these regions develops from being defined by local, anatomical proximity during childhood to being defined by distributed functional roles in adulthood (Fair et al., 2007, Fair et al., 2008, Fair et al., 2009, Kelly et al., 2009, Power et al., 2010, Supekar et al., 2009). Thus, development of cognitive control can be described as going from distributed networks of brain regions characterized by localized connections to more functionally central networks of brain regions characterized by long-distance connections. While evidence from these developmental studies suggests that the ability to overcome task set inertia will exhibit a similar developmental trajectory, it is still not yet known whether this is the case. For example, it is not known whether adolescents engage a similar, more frontally localized network as adults to overcome task set inertia, or if adolescents recruit a more distributed network containing both cortical and subcortical regions. Answering this question will have important implications for understanding the relationships between predominantly cortical versus subcortical systems of neurocognitive development.

We present behavioral and functional MRI results from a relatively large sample of 134 healthy adolescents and adults performing a novel attribute set switching task (SST). The primary study goal was to identify the neural correlates of task set inertia and to distinguish them from general set shifting brain function. We constructed a novel fMRI paradigm that systematically manipulated the interval between the end of one trial and the cue heralding the next to experimentally increase or decrease task set inertia. Importantly, the fMRI task design controlled for task set reconfiguration by fixing the cue-to-target interval. It, additionally, kept task–response rules constant and balanced the probability of each task, each response, and stimulus characteristics to ensure that neural effects were specific to task set inertia. We hypothesized that parametric analysis of response-to-cue interval (RCI) would reveal a subset of brain regions observed in previous fMRI comparisons between switch and non-switch trials studies specifically engaged to resolve residual interference between competing mental sets. Based on previous neuroimaging work (Loose et al., 2006), as well as behavioral work linking task set inertia to passive decay of previous task sets from working memory (Allport et al., 1994), we anticipated that these brain regions would include regions in the frontal cortices. Additionally, given inconsistent previous set switching findings for activity in subcortical regions we considered whether striatal engagement in set shifting may be related more to overcoming task set inertia. In order to ensure that we had the statistical power to detect any unique effects of overcoming task set inertia, we recruited a sample size much larger than previous set shifting functional neuroimaging studies. Our secondary goal was a cross-sectional analysis of age effects on task set inertia behavioral and neural effects. We aimed to characterize the developmental trajectory of task set inertia, which has not been previously examined. Our analyses again separately examined generalized switching effects and task set inertia effects. Because switching is thought to be one of the last executive functions to fully mature (Anderson, 2002), we hypothesized that late-maturing frontal lobe cortical regions would exhibit increased activity with age, with the most noticeable increases related to overcoming task set inertia. We also hypothesized that older participants would require less reliance on subcortical and lower level sensory cortical involvement to overcome residual set interference on switch trials, presumably because maturing prefrontal networks would not require basal ganglia and other related systems to inhibit competing response tendencies.

In summary, this study aimed to identify the neural correlates of task set inertia and distinguish them from those related to switching, and to characterize the developmental trajectory of task set inertia during adolescence. This was accomplished through: 1) comparison of the neural correlates of task set inertia and general main effects of shifting versus non-shifting task performance and 2) multivariate analyses of the effects of age on both switching and task set inertia.