Trait Anxiety Modulates the Neural Efficiency of Inhibitory Control

Abstract

Abstract■ An impairment of attentional control in the face of threat-related distracters is well established for high-anxious individuals. Beyond that, it has been hypothesized that high trait anxiety more generally impairs the neural efficiency of cognitive processes requiring attentional control-even in the absence of threat-related stimuli. Here, we use fMRI to show that trait anxiety indeed modulates brain activation and functional connectivities between task-relevant brain regions in an affectively neutral Stroop task. In high-anxious individuals, dorsolateral pFC showed stronger task-related activation and reduced coupling with posterior lateral frontal regions, dorsal ACC, and a word-sensitive area in the left fusiform gyrus. These results support the assumption that a general (i.e., not threat-specific) impairment of attentional control leads to reduced neural processing efficiency in anxious individuals. The increased dorsolateral pFC activation is interpreted as an attempt to compensate for suboptimal connectivity within the cortical network subserving task performance. ■

Anxious personality and functional efficiency of the insular-opercular network: A graph-analytic approach to resting-state fMRI

“…Studies have shown that anticipatory worry correlates with task-elicited activity and glucose consumption in dorsolateral prefrontal cortex (Tillfors, Furmark, Marteinsdottir, & Fredrikson, 2002). Furthermore, task fMRI studies point toward aberrant functional interactions between prefrontal control regions and subcortical areas in highly anxious participants (Basten et al, 2011;Bishop, Duncan, Brett, & Lawrence, 2004), and evidence from structural tractography suggests that individual differences in prefrontal-subcortical white matter projections represents a neurostructural correlate of anxiety . Although the insular-opercular network has been most dominantly implicated in anxiety (Vaidya & Gordon, 2013), other resting-state networks such as the frontoparietal control network comprising the dorsolateral prefrontal cortex, medial anterior cingulate, and the intraparietal lobule (Dosenbach et al, 2008) and the default-mode network have also been hypothesized to play a relevant role (Sylvester et al, 2012).…”

“…This might be relevant for the specification of neurobehavioral theories: A prominent psychological theory on attentional control, for instance, discusses the relevance of trait anxiety for processing efficiency, which refers to the relationship between the efforts or resources invested during task performance and the quality of task performance (Eysenck, Derakshan, Santos, & Calvo, 2007). Predictions of this theoretic account have been successfully tested using task fMRI (Basten et al, 2011), yet it remains unclear why trait anxiety would affect processing efficiency. One possible account would be suboptimal information exchange capability between relevant brain areas, which might be reflected in network efficiency as indexed by path lengths in relevant functional networks.…”

“…Task-based neuroimaging studies have shown that elevated levels of trait anxiety are associated with increased activity within the insular-opercular network (Hajcak, McDonald, & Simons, 2003;Most, Chun, Johnson, & Kiehl, 2006;Paulus, Rogalsky, Simmons, Feinstein, & Stein 2003). This stronger activation has been discussed as a compensatory mechanism for reduced processing efficiency, a claim backed up by the observation that activity increases are paralleled by decreases in within-network connectivity during task processing (Basten, Stelzel, & Fiebach, 2011).…”

“…As outlined earlier, decreased insular-opercular processing efficiency has been put forward as an explanation for increased reactivity of single parts of the network in highly anxious participants (Basten et al, 2011;Sylvester et al, 2012). Here, processing efficiency refers to the metabolic demands of a neural system to create a given output.…”

Interaction Effects of the COMT and DRD4 Genes with Anxiety-Related Traits on Selective Attention

“…It has been recently argued that trait anxiety is related to deficiencies in the executive control attentional network, while state anxiety is associated with hyperactivity of the alerting and orienting networks (Pacheco-Unguetti, Acosta, Callejas, & Lupianez, 2010). Consistent with ACT, neuroimaging studies demonstrated that high-anxious individuals had to invest more cognitive (compensatory) efforts in task performance which manifested itself as an increased task-related activation of the prefrontal cortex (PFC) (Ansari & Derakshan, 2011;Basten, Stelzel, & Fiebach, 2011;Eisenberger, Lieberman, & Satpute, 2005). At the same time, the reduced sustained activity of the PFC in high-anxious individuals was reported.…”