Elsevier

NeuroImage

Volume 59, Issue 2, 16 January 2012, Pages 1912-1923
NeuroImage

Impact of state anxiety on the interaction between threat monitoring and cognition

https://doi.org/10.1016/j.neuroimage.2011.08.102Get rights and content

Abstract

How does threat processing impact cognitive performance? To investigate this question, in the present functional magnetic resonance imaging study, participants performed a response-conflict task (neutral, congruent, and incongruent trials) that followed a variable-length shock anticipation period or a corresponding delay during which they would not be shocked. The delay period was cued by a geometric-shaped stimulus indicating whether the subject was in the safe (no shock) or threat (potential shock) condition. Behaviorally, participants showed increased reaction time interference (incongruent–neutral) during threat trials, an effect that increased as a function of state anxiety level across participants. Brain imaging data were analyzed for the cue and the subsequent target phase of the task. At the target phase, the left anterior insula exhibited interaction-type responses (i.e., increased interference during threat trials) that were positively associated with state anxiety level — a relationship that paralleled the behavioral pattern. At the cue phase, greater responses to threat vs. safe were observed in a circuit of regions, including the medial PFC, anterior insula, thalamus, and bed nucleus of the stria terminalis/caudate, which we interpreted as engaged by shock monitoring/anticipation processes. In contrast, intriguingly, greater responses to safe vs. threat at the cue phase were observed in a broader set of regions that overlapped with the “resting-state” network. Finally, a standard statistical mediation analysis revealed that the relationship between state anxiety scores and interference-related responses in the left anterior insula during the target phase was partially mediated via cue responses in the medial PFC, consistent with the idea that more anxious individuals had difficulty in engaging the medial PFC during the threat condition. Taken together, our findings suggest that threat monitoring impairs the upcoming resolution of interference. Furthermore, a confluence of effects of cognitive task condition, threat, and individual differences in state anxiety was observed in the anterior insula, a structure that is suggested to be particularly important for the interaction between emotion and cognition.

Highlights

► We investigated how shock monitoring affects subsequent conflict processing. ► Shock monitoring affected conflict processing at both behavioral and neural levels ► State anxiety modulated the interaction between shock monitoring and conflict. ► This three-way interaction was observed in the anterior insula. ► Shock anticipation engaged the medial PFC, thalamus, anterior insula, and the BNST.

Introduction

In the past decade, a growing body of studies has investigated the impact of emotional stimuli on cognitive function. For instance, in a working memory task, negative distractors impair behavioral performance to a larger extent than neutral items (Anticevic et al., 2010, Dolcos and McCarthy, 2006). The impact of emotion on many other cognitive tasks has been investigated, including conflict processing (Blair et al., 2007, Hart et al., 2010, Kanske and Kotz, 2010) and response inhibition (Pessoa et al., in press). This literature has focused on paradigms in which the role of emotion is closely associated with a stimulus (typically an unpleasant picture). Another central property of these paradigms is that the temporal characteristics of the emotional stimulus are generally known to the participants and fixed.

At the same time, recent studies have attempted to understand the impact of more temporally extended emotional manipulations, so as to approximate conditions that are closer to anxiety than fear (Davis et al., 2010). Along these lines, in the present study, our goal was to investigate cognitive performance subsequent to a period of shock anticipation. Participants performed a cognitive task during two experimental contexts (Fig. 1). An initial cue stimulus signaled whether the trial was “safe” or “threat”. During threat trials, mild electric shock was administered to participants in a third of the trials during a variable-length delay period in a way that the timing of the shock was unpredictable to participants. During safe trials, the trial timing and structure were the same, except that no shocks were administered. Following the anticipation period, participants were asked to determine if a picture contained a house or building while ignoring task-irrelevant words, which were used to create neutral, congruent, and incongruent trials — we refer to this latter task period as the “target” phase.

We hypothesized that monitoring for a potential shock affects task performance via its impact on capacity-limited information processing — much like strong emotional stimuli, as suggested in the dual competition framework (Pessoa, 2009). Accordingly, shock monitoring would use processing resources needed for subsequent conflict processing, thereby having its largest impact on incongruent trials, during which response conflict must be adequately resolved to ensure correct task behavior.

As shown in Fig. 1, the task was designed such that the cue and target phases were separated by a short, variable-length duration period. Whereas one goal of this manipulation was to generate temporal uncertainty regarding potential shock delivery, a second goal was to allow us to independently estimate evoked responses to both task phases. Regarding the former, this allowed us to contrast responses evoked by the cue during trials that were structurally identical, except for the geometric shape of the cue stimulus (trials that actually contained a physical shock were discarded from the main analyses). Previous studies have identified a number of regions involved in threat monitoring, including dorsomedial prefrontal cortex (PFC), anterior insula, bed nucleus of the stria terminalis (BNST), and thalamus, among others (Chandrasekhar et al., 2008, Kalin et al., 2005, Mobbs et al., 2010, Somerville et al., 2010). The BNST is especially interesting given its potential involvement in monitoring escalating threat levels (see Davis et al., 2010 for a review). The anterior insula is also particularly relevant because it is critically involved in the processing of bodily signals and contains a visceral sensory cortex that maps the internal state of the body in a precise fashion (Craig, 2002, Craig, 2009). Accordingly, we anticipated that, in our task, threat as signaled by the cue stimulus would engage some of these regions.

A central goal of our study was to understand the impact of threat monitoring on responses evoked during task execution, which was possible, again, given that our design allowed separate estimation of target phase responses. The medial PFC has been suggested to have an important role in conflict processing and other effortful functions (Botvinick et al., 2001, Brown and Braver, 2005, Weissman et al., 2005). In a recent study, conflict-related responses in medial PFC decreased during trials in which participants could earn a reward for fast and accurate performance (Padmala and Pessoa, 2011). In the present experiment, instead, we expected that conflict-related responses in medial PFC would increase during the threat condition (vs. safe) — because threat was expected to increase response interference. A region of particular interest during the target phase was, again, the anterior insula, which not only is strongly implicated in emotional processing, but also during cognitive function. Indeed, the anterior insula is consistently engaged during a range of cognitive tasks (Dosenbach et al., 2006, Van Snellenberg and Wager, 2009). Given that both shock monitoring and response conflict were involved in our task, the anterior insula might constitute a site where emotional and cognitive information interact.

Finally, we were interested in understanding how individual differences influenced both behavioral performance and brain responses. Behaviorally, we anticipated that greater response interference would be observed in participants with higher state and/or trait anxiety. Brain responses were also anticipated to vary based on individual differences during the cue and target phases of the task. In particular, the medial PFC and thalamus are involved in the regulation of anxiety-related behaviors in non-human primates (e.g., Kalin et al., 2005). Human neuroimaging studies have described the engagement of the medial PFC during emotion regulation, too (Banks et al., 2007; for review Ochsner and Gross, 2005). If, during our task, these structures also performed regulatory functions, their recruitment during the cue phase could also vary as a function of state/trait anxiety. In particular, participants with higher levels of anxiety might exhibit weaker cue-related responses in these regions, possibly reflecting the participant's inability to adequately regulate their emotion. In addition, of particular interest was the possibility that cognitive–emotional interactions during the target phase depended on individual differences, too. In this scenario, the interaction between shock monitoring and response interference would be a function of state/trait anxiety levels — e.g., an emotion × cognition statistical interaction would be evident for high- but not low-anxious individuals.

Section snippets

Subjects

Forty-seven volunteers participated in the study, which was approved by the Institutional Review Board of Indiana University, Bloomington. Participants were screened during the recruitment process based on self-reports concerning the following items: not be taking psychoactive drugs (including Zoloft, Ritalin, and drugs of abuse); have no known psychological condition (including ADD, depression, PTSD, and clinical anxiety); and have no known neurological condition (including stroke, seizure,

Skin conductance responses

Skin conductance responses revealed that responses were greater during trials involving shock monitoring relative to safe ones [mean (STD) in log-transformed units: .019 (.019) during threat and .003 (.009) during safe]. Indeed, a paired t test revealed a significant difference (t37 = 4.53, p < .001), indicating that the shock manipulation was successful.

Behavioral results

Reaction time data (Fig. 2A) were evaluated according to a 2 Monitoring (safe, threat) × 3 Congruency (neutral, congruent, incongruent)

Discussion

In the present study, we investigated how threat affected subsequent response-conflict processing. Behaviorally, a threat monitoring by response conflict interaction was observed in that interference (incongruent vs. neutral RT) was increased following threat monitoring. These interaction effects were positively related to state anxiety scores across individuals — the higher the state anxiety, the larger the interference during the threat condition. The neuroimaging findings also revealed

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