Anxiety, a benefit and detriment to cognition: Behavioral and magnetoencephalographic evidence from a mixed-saccade task
Highlights
► Subjects performed a mixed-saccade task under anxiety-provoking conditions. ► Threat of shock impeded anti-saccades, but facilitated reflexive pro-saccades. ► Enhanced lateral frontal cortical theta preceded correct anti-saccades under threat. ► Parietal beta desynchronization preceded efficient saccade execution. ► Anxiety may reduce cognitive flexibility by promoting stimulus-driven responding.
Introduction
Cognitive models of anxiety emphasize anxiety’s detrimental effects on cognitive-behavioral performance (Bishop, 2007, Eysenck and Calvo, 1992, Eysenck et al., 2007). High-anxious participants show disturbances in prefrontally-mediated processes such as goal-directed control of attention (Bishop, Jenkins, & Lawrence, 2007). These attention control disturbances may stem directly from inherent executive dysfunction and underlying abnormalities in prefrontal cortices (Bishop, 2008). An alternative view emphasizes adaptive functions of anxiety, defined as heightened action readiness in the face of ambiguous, unpredictable threat. Anxiety may constrain goal-directed attention mechanisms, but only secondarily as priorities are shifted to monitoring the environment and being maximally receptive to potential threat signals, irrespective of competing task demands (Cornwell et al., 2011). Two hypotheses emerge from this latter standpoint, and promote a broader view of anxiety’s effects – positive and negative – on cognition (see also Eysenck et al., 2007, Pessoa, 2009). First and foremost, anxiety facilitates reflexive and habitual, over-learned behaviors that rely on stimulus-driven attention mechanisms. Second and as a consequence, anxiety hinders novel, flexible behavior, particularly that which competes with the former.
The mixed-saccade task – which pits habitual actions (pro-saccades) against atypical actions (anti-saccades) – provides an ideal platform to test these hypotheses. Despite both being volitional responses in this task, pro-saccades are congruent with, while anti-saccades compete with and demand suppression of, the habitual tendency to target the eyes toward a suddenly appearing object. This task has figured prominently in research on various psychopathological conditions such as schizophrenia and attention-deficit/hyperactivity disorder (for a review, see Hutton & Ettinger, 2006). Recent work has shown that anxiety is associated with impaired anti-saccade performance, further linking anxiety with poor cognitive-behavioral performance (Ansari et al., 2008, Derakshan et al., 2009, Jazbec et al., 2005, Wieser et al., 2009; but see Ettinger et al., 2005). However, no evidence was provided for anxiety-related improvements in pro-saccade performance. Such evidence would bolster the hypothesis that anxiety facilitates stimulus-driven actions, which, in turn, hinder competing actions. In these studies, participants were grouped by pre-existing anxiety characteristics (e.g., trait anxiety). Anxiety was not manipulated, leaving open the possibility that group differences were driven by dispositional attributes other than anxiety.
Experimentally manipulating anxiety, as we did here, allows direct attribution of changes in cognitive-behavioral performance to concurrent anxiety states and may provide a more sensitive means to study the broader impact of anxiety on cognition (Lavric et al., 2003, Shackman et al., 2006, Vytal et al., in press). Healthy volunteers performed visually-elicited pro-saccades and anti-saccades under two conditions: (1) during periods of risk of receiving aversive electric shocks and (2) during periods of safety. Threat of shock is a robust method for inducing sustained anxiety in healthy individuals (Cornwell et al., 2007, Grillon, 2002). Threat-induced anxiety sensitizes sensory-perceptual processing as evidenced by increased cortical and midbrain responses to innocuous stimuli when participants anticipate shock (Baas et al., 2006, Cornwell et al., 2007). Arguably, this leads to increased stimulus-driven attention capture (Cornwell et al., 2008, Grillon and Davis, 1997), which, in the present context, should be beneficial to performing pro-saccades but detrimental to performing anti-saccades. Accordingly, we hypothesized greater divergence (opposite effects) in pro- vs. anti-saccade performance (i.e., onset latency) under threat-induced anxiety relative to safe, non-anxious conditions. This divergence was expected to reflect a combination of a facilitating effect on initiating pro-saccades and a hindering effect on initiating anti-saccades under threat.
Neural correlates of anxiety’s effects on pro-saccade or anti-saccade performance have not received much attention, heretofore (Ansari & Derakshan, 2011). To fill this gap, we recorded brain oscillations with whole-head magnetoencephalography (MEG). Specifically, we examined spectral power during saccade preparation (i.e., before saccade execution) in the interval between the instruction cue (pro- or anti-saccade) and target presentation. This time window was selected for analysis because electrophysiological data in humans and nonhuman primates point to an important role of neuronal activity during saccade preparation in tuning saccade pathways for optimal execution of an upcoming pro-saccade or anti-saccade (Dorris et al., 1997, Everling et al., 1998, Mueller et al., 2009, Munoz and Everling, 2004). It has also been recently shown that neural activity preceding anti-saccades differs between high and low anxious participants (Ansari & Derakshan, 2011). MEG, unlike other neuroimaging techniques such as functional MRI, has the prerequisite temporal resolution to isolate this preparatory activity from activity mediating visual target detection and saccade execution (Herdmann and Ryan, 2007, Hinkley et al., 2011, Sestieri et al., 2008). Adaptive MEG beamformer analyses (i.e., synthetic aperture magnetometry, SAM, Vrba & Robinson, 2001) were performed to estimate oscillatory power in key regions involved in controlling saccades and/or attention: frontal eye fields, supplementary eye fields, dorsolateral prefrontal cortices, dorsal anterior cingulate, inferior parietal cortices and superior colliculi (Chikazoe et al., 2007, Corbetta et al., 2008, Luna et al., 1998, Munoz and Everling, 2004).
The dorsal fronto-parietal cortical network mediating volitional saccades has also been implicated, more generally, in goal-directed attention control (Corbetta and Shulman, 2002, Corbetta et al., 2008). This dorsal attention system, as argued by Corbetta and colleagues, can be partially dissociated from a right-lateralized ventral fronto-parietal cortical system – comprised of right ventrolateral prefrontal and temporoparietal cortices – that mediates stimulus-driven attention. It is this ventral attention system that we hypothesize must be down-regulated for participants to effectively suppress reflexive pro-saccades to correctly execute anti-saccades under threat-induced anxiety, when sensory-perceptual systems are sensitized and stimulus-driven attention capture is likely optimized (Vuilleumier & Driver, 2007). Thus, ventral cortical structures involved in stimulus-driven attention should be distinctly modulated on anti-saccade trials under threat. Threat-related modulation of activity in dorsal cortical structures mediating goal-directed attention and volitional control of saccades was also anticipated, but no specific predictions were made. We focused on theta (4–8 Hz), alpha (8–12 Hz), and beta (14–30 Hz) oscillatory activity within these regions of interest.
Section snippets
Participants
Twenty healthy adult volunteers participated in both a MEG testing session and a separate session to obtain an anatomical MRI for source analysis. Data from three participants were discarded due to either excessive head movement during the MEG scan or significant eye movement artifacts recordings, leaving a final sample of 17 participants (10 men, 7 women, mean age = 27 yr, range = 22–34 yr). Exclusion criteria included: (1) past or current psychiatric disorders as per the Structured Clinical
Subjective and physiological arousal
Higher mean subjective anxiety was reported for Threat (Mean ± SD, 4.96 ± 1.84 AU) relative to Safe (1.87 ± 1.36 AU), t(16) = 6.99, p < .001. In addition, there was a greater mean change in heart rate following onset of Threat (2.89 ± 2.18 bpm) compared to Safe (1.90 ± 2.84 bpm), t(16) = 2.21, p = .04.
Saccade performance
Mean raw onset latencies and error rate data are presented in Table 1. For log10-transformed mean (correct) saccade onset latencies, a 2 × 2 × 2 repeated-measures ANOVA, with Context (safe, threat), Saccade (pro-saccade,
Discussion
Our results confirm that threat of shock reliably elicits sustained anxiety, and they support its use as a means to examine the effects of state anxiety on neurocognitive processes. As expected, participants reported increased anxiety and showed increased heart rate under threat relative to safety. Within this threat-induced anxiety state, both saccade performance and neural oscillatory activity preceding saccades were affected. Although threat of shock loomed equally large over all trials,
Conclusion
It is clear from these data that anxiety has multifaceted effects on cognition and underlying brain processes. Threat-induced anxiety impaired flexible responding (anti-saccades) but enhanced stimulus-driven responding (pro-saccades), at least the kind thought to be reflexive (erroneous pro-saccades). Instead of pointing to inherent dysfunction of prefrontal-based executive mechanisms, evidence from MEG source analyses emphasizes the need to constrain stimulus-driven mechanisms – perhaps by
Funding
This work was supported by the Intramural Research Program of the National Institute of Mental Health (NIMH) at the National Institutes of Health (NIH).
Acknowledgment
We wish to thank all members of the NIMH Magnetoencephalography Core for their technical support and assistance.
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