Unraveling the anxious mind: anxiety, worry, and frontal engagement in sustained attention versus off-task processing

Abstract

Much remains unknown regarding the relationship between anxiety, worry, sustained attention, and frontal function. Here, we addressed this using a sustained attention task adapted for functional magnetic resonance imaging. Participants responded to presentation of simple stimuli, withholding responses to an infrequent "No Go" stimulus. Dorsolateral prefrontal cortex (DLPFC) activity to "Go" trials, and dorsal anterior cingulate (dACC) activity to "No Go" trials were associated with faster error-free performance; consistent with DLPFC and dACC facilitating proactive and reactive control, respectively. Trait anxiety was linked to reduced recruitment of these regions, slower error-free performance, and decreased frontal-thalamo-striatal connectivity. This indicates an association between trait anxiety and impoverished frontal control of attention, even when external distractors are absent. In task blocks where commission errors were made, greater DLPFC-precuneus and DLPFC-posterior cingulate connectivity were associated with both trait anxiety and worry, indicative of increased off-task thought. Notably, unlike trait anxiety, worry was not linked to reduced frontal-striatal-thalamo connectivity, impoverished frontal recruitment, or slowed responding during blocks without commission errors, contrary to accounts proposing a direct causal link between worry and impoverished attentional control. This leads us to propose a new model of the relationship between anxiety, worry and frontal engagement in attentional control versus off-task thought.

Keywords: anxiety; frontal function; off-task thought; sustained attention; worry.

Figure 1.

The sustained attention to response task (SART), adapted for functional magnetic resonance imaging (fMRI). In SART blocks, participants responded by key press to all digits except the digit “3”, these “No Go” trials were infrequent (2 or 3 per block of 28). In Control blocks, participants responded by key press to all letters; in these blocks there were only “Go” trials.

Figure 2.

Trait anxiety was associated with reduced activity in both dorsal ACC and right DLPFC ROIs for SART No Go trials versus baseline (the BOLD signal was averaged across each ROI for each participant). dACC, dorsal anterior cingulate cortex; DLPFC, dorsolateral prefrontal cortex; SART, Sustained Attention to Response Task.

Figure 3.

Anxiety, DLPFC activation and SART performance. (a) Right DLPFC activity on SART Go trials - Control Go trials is plotted against STAI trait anxiety as a function of block type (EF, commission Error-Free; EM, commission Error-Made; C, Control). (b) To illustrate this result further, we used a median split on STAI trait anxiety scores to show DLPFC activation on Go trials by block type (Sart Error-Free, Sart Error-Made, Control) and anxiety level (low, high). Trial-specific activity is calculated against the implicit baseline. (c) DLPFC activation on Go trials in Error-Free (vs. Control) blocks is linked to faster error-free performance. (d) Trait anxiety, in turn, is linked to slower error-free performance. DLPFC, dorsolateral prefrontal cortex; SART, Sustained Attention to Response Task; STAI, Spielberger State Trait Anxiety Inventory.

Figure 4.

Results from psychophysiological interaction (PPI) based functional connectivity analyses of DLPFC seeded connectivity as a function of block type and STAI trait anxiety. Trait anxiety was significantly associated with decreased connectivity between right DLPFC and bilateral caudate (a) and thalamus (b) ROIs across Go trials in Error-Free (EF) versus Control (C) blocks. No significant association between trait anxiety and connectivity between these regions was observed in Error-Made versus Control blocks. In addition, trait anxiety was significantly associated with increased connectivity between right DLPFC and bilateral precuneus (c) and posterior cingulate (d) ROIs across Go trials in Error-Made (EM) versus Control (C) blocks. There was no significant association between trait anxiety and connectivity between these regions in Error-Free versus Control blocks. DLPFC, dorsolateral prefrontal cortex; STAI, Spielberger State Trait Anxiety Inventory.

Figure 5.

Relationship between worry and frontal function. (a) PSWQ worry scores correlated positively with DLPFC activity on Go trials in the Error-Made (EM) versus Control (C) blocks, showing a similar but stronger relation to trait anxiety, and statistically mediating the relationship between STAI trait scores and this index of DLPFC activity. (b) Unlike trait anxiety, worry (PSWQ scores) did not show a significant relationship with DLPFC activation on Go trials during SART Error-Free (EF) versus Control (C) blocks. (c,d) Worry (PSWQ scores) was associated with increased connectivity between DLPFC and Default Mode regions—precuneus (c) and posterior cingulate (d) across Go trials in SART Error-Made (EM) versus Control (C) blocks. There was no significant association between worry and DLPFC connectivity with thalamus and caudate for Go trials during Error-Free (EF) versus Control (C) blocks. DLPFC, dorsolateral prefrontal cortex; SART, Sustained Attention to Response Task; STAI, Spielberger State Trait Anxiety Inventory; PSWQ, Penn State Worry Questionnaire.

Figure 6.

Illustration of the proposed relationship between trait anxiety, worry, attentional control, and generation of spontaneous self-referent thoughts. In this model, trait anxiety is associated with both impoverished attentional control and increased worry, the latter being in turn linked to elevated levels of spontaneous thoughts about personal concerns. The attentional control dimension is held to entail reduced engagement of DLPFC in a frontal-thalamo-striatal network that supports the proactive control of attention, as well as reduced ACC and DLPFC engagement in reactive control (not shown here). The worry/spontaneous thought dimension is held to entail increased interaction between DLPFC and Default Mode regions implicated in self-referent processing, in particular the precuneus and posterior cingulate. Of note, worry is not directly associated with impoverished attentional control. A possibility that requires additional investigation is that individual variation in both these dimensions might contribute to the extent to which disruptive task-unrelated mind-wandering, focused on self-related concerns, occurs during attempts to perform everyday tasks. DLPFC, dorsolateral prefrontal cortex; ACC, anterior cingulate cortex.