Abstract
Individuals with high-trait anxiety frequently report decreased perceived control. However, it is unclear how these processes are instantiated at a neural level. Prior research suggests that individuals prone to anxiety may have exaggerated activity in the anterior insula and altered activity in the cingulate cortex during anticipation of aversive events. Thus, we hypothesized that anxiety proneness influences anterior insula activation during anticipation of unpredictable threat through decreased perceived control. Forty physically healthy adults underwent neuroimaging while they explored computer-simulated contexts associated either with or without the threat of an unpredictable shock. Skin conductance, anxiety ratings and blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging were used to assess responses to threat versus no threat. Perceived control was measured using the Anxiety Control Questionnaire-Revised. Mediation analysis examined how anxiety proneness influenced BOLD activity. Anticipation of unpredictable threat resulted in increased skin conductance responses, anxiety ratings and enhanced activation in bilateral insula, anterior midcingulate cortex (aMCC) and bed nucleus of the stria terminalis. Individuals with greater anxiety proneness and less perceived control showed greater activity in dorsal anterior insula (dAI). Perceived control mediated the relationship between anxiety proneness and dAI activity. Increased dAI activity was associated with increased activity in aMCC, which correlated with increased exploratory behavior. Results provide evidence that exaggerated insula activation during the threat of unpredictable shock is directly related to low perceived control in anxiety-prone individuals. Perceived control thus may constitute an important treatment target to modulate insula activity during anxious anticipation in anxiety-disordered individuals.
Highlights
Trait anxiety, a predisposition to respond anxiously, has been linked to dysregulation of mood and anxiety,[1] but the underlying brain processes by which anxiety proneness affects neural systems remain unclear
These prior reports suggest that the insula is broadly involved in anxious anticipation, studies that have compared anticipation of temporally predictable and unpredictable aversive events indicate that activity in anterior insula is heightened during anticipation of unpredictable aversive events compared with predictable aversive events.[15,16]
Several studies report that nonclinical subjects with high trait anxiety compared with those having low-trait anxiety show enhanced activation in anterior insula during emotional processing and the anticipation of aversive images.[29,30,31]. These results indicate that individuals with dysregulated mood or anxiety because the bed nucleus of the stria terminalis (BNST) has been implicated in modulating sustained anxiety responses analogous to those elicited to a context in which an aversive event may occur that otherwise is unpredicted by any sensory cue,[17,44] and in preclinical and clinical studies of the functional anatomy of sustained apprehensive states,[45] we examined activity in the BNST
Summary
A predisposition to respond anxiously, has been linked to dysregulation of mood and anxiety,[1] but the underlying brain processes by which anxiety proneness affects neural systems remain unclear. Several studies report that nonclinical subjects with high trait anxiety compared with those having low-trait anxiety show enhanced activation in anterior insula during emotional processing and the anticipation of aversive images.[29,30,31] These results indicate that individuals with dysregulated mood or anxiety because the bed nucleus of the stria terminalis (BNST) has been implicated in modulating sustained anxiety responses analogous to those elicited to a context in which an aversive event may occur that otherwise is unpredicted by any sensory cue,[17,44] and in preclinical and clinical studies of the functional anatomy of sustained apprehensive states,[45] we examined activity in the BNST. Manifest altered activity in anterior insula during the anticipation of aversive events
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