ReviewMeta-analysis of the neural correlates of vigilant attention in children and adolescents
Introduction
Vigilant attention (VA) is a critical cognitive function that plays a major role in everyday tasks such as driving a car or following a conversation. In the field of cognitive psychology, the term VA has been defined as the ability to maintain focused attention during cognitively unchallenging and redundant tasks for a prolonged period of time (Robertson & Garavan, 2004). This definition has been further developed by Langner and Eickhoff (2013) as a ‘process of maintaining efficient conscious stimulus processing over periods ranging from 10 seconds up to several minutes’. The VA function is generally thought to be supported by top-down or endogenous processes that are driven by internal goals and enable one to voluntarily maintain or focus attention. It is opposed to bottom-up or exogenous processes that are driven by external stimuli in the environment, although a strong interaction between endogenous and exogenous processes have been shown to occur in vigilance tasks (Maclean et al., 2009). This interaction is accompanied by a decrease in performance over time, the so-called vigilance decrement (Fortenbaugh, Degutis, & Esterman, 2017).
Although the nature and factors underlying VA have been investigated over the past few decades, notably in adults, there has been little research on the development of this complex cognitive process across the lifespan. Nevertheless, a recent cohort study examined VA-related measures in 10,000 participants (Fortenbaugh et al., 2015) using a version of the Continuous Performance Task (CPT) which is a commonly-used task measuring VA-related abilities (Riccio, Reynolds, Lowe, & Moore, 2002). Typically, this test assesses vigilant responses to infrequently occurring stimuli. Fortenbaugh and colleagues (2015) found that VA performances rapidly improves from 10 to 16-years of age. This ability then improves more steadily throughout adulthood before declining in late adulthood. The authors proposed that shifts in response speed and carefulness may underlie changes in VA abilities across the lifespan. Similarly, another study detected a U-shaped developmental trend in VA abilities in 113 individuals from 12 to 75 year-old, describing low performances in childhood and adolescence, a plateau in performance in adulthood and a decrease in performance in older adulthood (Mcavinue et al., 2012). According to the latter study, attentional abilities are relatively conserved in older adults and this population likely relies more on top-down attentional control to compensate for decline in sensory function.
Regarding the development of VA-related abilities during childhood, a recent study found that improvements in VA-related measures are age-dependent (Lewis, Reeve, Kelly, & Johnson, 2017). Using a sustained attention task to assess several VA-related measures, such as reaction time variability and omission errors (i.e., non-response to target of interest), in children aged 6 to 10-years, Lewis et al. (2017) showed that younger children (i.e., 6-7 years of age) performed poorly relative to older children (i.e., 8-10 years of age) and had time-on-task effects in all measures, whereas older children seemed to reach a relative steadiness in performance between 8 and 9-years of age. This provides additional support to previous behavioural findings showing steady and age-dependent improvements in VA performances in young populations (Betts, Mckay, Maruff, & Anderson, 2006; Lin, Hsiao, & Chen, 1999). Collectively, these studies show that there is a rapid improvement of VA abilities throughout childhood and adolescence before reaching a plateau in young adulthood and peaking in the mid-40's. These VA abilities tend to gradually decline in late adulthood. An age-related change in strategy to maintain attention over prolonged periods of time may account for the development of the VA functions across the lifespan.
Although some behavioural studies have investigated the developmental trajectory of VA performances, little is known about the neural correlates of this cognitive function in neurotypical children and adolescents. Recently, a study applied a brain network maturational growth method in 519 young participants, including 25 subjects with Attention Deficit/Hyperactivity Disorder (ADHD), to investigate the maturation of interrelationships between intrinsic connectivity networks (ICNs) thought to be involved in attentional abilities (Kessler, Angstadt, & Sripada, 2016). The authors demonstrated that subjects who deviated the most from the normative maturational curve had the worst VA performances, corroborating previous assumptions that large-scale ICNs contribute to the effective maintenance of attentional functions (Castellanos & Proal, 2012). Another functional magnetic resonance imaging (fMRI) study investigated the neural substrates underlying the alerting system, comparable to VA, in a sample of neurotypical children (Konrad et al., 2005). Although the behavioural task did not specifically assess VA performances, the authors found an increased activation of the superior temporal gyrus and middle occipital cortex in children in the alerting condition suggesting an involvement of these brain regions during VA tasks. Recently, O'Halloran and colleagues (2018) investigated the brain regions associated with good performance in sustained attention in healthy children and children with ADHD. They showed that good VA performance as assessed by intra-individual response time variability was associated on average with increased activation of the bilateral insula, anterior cingulate cortex and prefrontal regions. Using a sustained attention task, an fMRI study sought to examine the neurodevelopmental substrates of sustained attention between childhood and adulthood (Smith, Halari, Giampetro, Brammer, & Rubia, 2011). The findings showed that increased activation in right inferior frontal and temporo-parietal regions during the sustained attention task was positively correlated with increasing age.
In order to assess the brain regions underlying VA in young neurotypical subjects, the current meta-analysis will examine the fMRI studies that used behavioural tasks thought to engage the maintenance of high attentional demands over a prolonged period of time to complete the task at hand. These tasks are categorized into two main paradigms. First, the continuous performance tests, including the CPT and Oddball task, which require responses to infrequently occurring visual or auditory stimuli (Huettel & Mccarthy, 2004; Losier, Mcgrath, & Klein, 1996; Riccio et al., 2002). Alternatively, variants of the CPT, such as the Conner's CPT, require continuous responding and has gained much interest in studies on VA (Conners, Epstein, Angold, & Klaric, 2003; Macqueen et al., 2018). Second, the go/no-go paradigm which requires participants to respond quickly to frequent stimuli and to withhold their response to infrequent target stimuli (Wright, Lipszyc, Dupuis, Thayapararajah, & Schachar, 2014). Traditional go/no-go tasks encompass the Stop Signal Task (SST) and the common Go/No-go task. The no-go condition of these tasks has been commonly manipulated to assess inhibition processes in participants. However, some authors have argued that the ability to detect no-go signals over time requires high attentional demands and the maintenance of attention to rare target stimuli (Criaud & Boulinguez, 2013; Hwang et al., 2019; Li, Huang, Constable, & Sinha, 2006). Notably, it has been suggested that critical confounds, such as the low frequency of the no-go signals (i.e., target signal), may involve sustained attention (Criaud & Boulinguez, 2013). Thus, the design of go/no-go tasks with rare no-go signals is similar to the traditional design of VA tasks that generally consist of a higher ratio of non-target signals than target signals (Langner & Eickhoff, 2013).
The current study aims to meta-analytically define the neural correlates of VA in neurotypical children and adolescents reviewing and examining previous fMRI studies which used behavioural tasks involving VA-related abilities. Based on previous studies in children and adults (Christakou et al., 2013; Chun, Golomb, & Turk-Browne, 2011; Coull, Frith, Frackowiak, & Grasby, 1996; Langner & Eickhoff, 2013; Smith et al., 2011), it is hypothesized that the meta-analysis will reveal a set of brain regions located in frontal, cingulate and parieto-temporal areas.
Section snippets
Search strategies
A search was performed using three electronic databases: PubMed, Google scholar and ScienceDirect. fMRI studies published before April 2019 were selected. The search terms were [vigilant attention or sustained attention or tonic attention or alertness] and [children or adolescent] and [functional MRI or fMRI or functional magnetic resonance imaging] in combination with [CPT or continuous performance task or go/no-go or Oddball or Stop-signal task]. The search was extended to studies which were
Results
Overall, 25 studies encompassing 25 experiments (ratio 1:1) were included with the average age across all experiments being 12.89 ± 2.26 years (72% male; 96% right handed). From the 25 experiments there were a total of 223 foci (Table 1). In one study, the control group was neurotypical children with orthopedic injuries (N = 8). An additional analysis was conducted with this study excluded (Supplementary material; Table S1), however, the results were similar to the general ALE analysis.
The ALE
Discussion
The present meta-analysis included 25 fMRI studies that used different behavioural paradigms assessing, but not limited to, VA. There were five mainly right-lateralized neural clusters that involved the right medFG extending to the SFG and cingulate gyrus, the bilateral STG, the right SFG and right IFG. This is consistent with the VA-related brain regions identified in adults (Langner & Eickhoff, 2013) and previous literature on the neural correlates of attention, and more specifically, VA (
Limitations
The present meta-analysis identified the brain clusters related to VA in children and adolescents using different cognitive tasks. Firstly, although the current study aimed to analyze the neural correlates of VA in children and adolescents, the mean age range was rather broad (8–17.99 year old). Given the continuous neurodevelopmental changes during childhood and adolescence, it is likely that the current VA network does not represent an age-dependent network. Further research is warranted
Conclusion
Overall, the investigation of the neural correlates of VA in children and adolescents yielded a convergence of mainly right-lateralized brain clusters. Although continuous and critical brain maturational processes occur during childhood and adolescence, the present VA network as observed in neurotypical children and adolescents shares some neural basis with the VA network as identified in adults. Given the complexity of this cognitive process, future studies investigating the neural correlates
Author contribution statement
H.M. and F.Z. conceptualized the present work. H.M., T.S. and K.G. designed the methodology. H.M. collected the data and performed the analysis. F.Z., P.R. and S.H. helped supervise the project. All authors contributed to the interpretation of the results and writing of the manuscript. H.M., T.S., K.G. and P.R. reviewed and edited the final manuscript.
Declaration of Competing Interest
The authors declare no competing financial interests.
Acknowledgements
The first author is a recipient of a University Postgraduate Award and Australian Government Research Training Program Scholarship at The University of Western Australia. We thank Mick Fox for his suggestions and software support.
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Asterisks designate studies included in the meta-analysis.