Abstract
Acute stress is known to induce a state of hypervigilance, allowing optimal detection of threats. Although one may benefit from sensitive sensory processing, it comes at the cost of unselective attention and increased distraction by irrelevant information. Corticosteroids, released in response to stress, have been shown to profoundly influence brain function in a time-dependent manner, causing rapid non-genomic and slow genomic effects. Here, we investigated how these time-dependent effects influence the neural mechanisms underlying selective attention and the inhibition of emotional distracters in humans. Implementing a randomized, double-blind, placebo-controlled design, 65 young healthy men received 10 mg hydrocortisone either 60 min (rapid effects) or 270 min (slow effects), or placebo prior to an emotional distraction task, consisting of color-naming of either neutral or aversive words. Overall, participants responded slower to aversive compared to neutral words, indicating emotional interference with selective attention. Importantly, the rapid effects of corticosteroids increased emotional interference, which was associated with reduced amygdala inhibition to aversive words. Moreover, they induced enhanced amygdala connectivity with frontoparietal brain regions, which may reflect increased influence of the amygdala on an executive network. The slow effects of corticosteroids acted on the neural correlates of sustained attention. They decreased overall activity in the cuneus, possibly indicating reduced bottom-up attentional processing, and disrupted amygdala connectivity to the insula, potentially reducing emotional interference. Altogether, these data suggest a time-specific corticosteroid modulation of attentive processing. Whereas high circulating corticosteroid levels acutely increase emotional interference, possibly facilitating the detection of threats, a history of elevation might promote sustained attention and thereby contribute to stress-recovery of cognitive function.
Highlights
Stress has profound influence on the brain’s attentional resources
The rapid effects of corticosteroids increased emotional interference, which was associated with reduced amygdala inhibition to aversive words
PHYSIOLOGICAL AND PSYCHOLOGICAL MEASURES As expected, oral administration of 10 mg hydrocortisone increased salivary cortisol levels to those observed during moderate-to-severe stress (Morgan et al, 2000) (Figure 1A), which was evidenced by a significant main effect of group [F(2, 62) = 41.63, p < 0.001] and a time × group interaction [F(18, 110) = 29.04, p < 0.001)
Summary
Stress has profound influence on the brain’s attentional resources. When exposed to an acutely stressful situation, the brain shifts into a mode of hypervigilant processing in which the detection and assessment of potential threats is optimized by prioritized sensory processing (de Kloet et al, 2005; van Marle et al, 2009), and the amygdala, key modulator of vigilance and emotional processing in the brain (Phelps and Ledoux, 2005), is activated (van Marle et al, 2009). This surge in vigilance in immediate response to stress is thought to be mediated by the central release of norepinephrine (NE) by tonic activation of the locus coeruleus (LC) (Aston-Jones and Cohen, 2005; Valentino and Van Bockstaele, 2008; Cousijn et al, 2010) This state of hypervigilance is highly adaptive and enhances chances of survival during stressful situations, but it comes at the cost of specificity (van Marle et al, 2009), impaired selective attention (Tanji and Hoshi, 2008; Henderson et al, 2012) and increased susceptibility to distraction (Skosnik et al, 2000; Braunstein-Bercovitz et al, 2001; Aston-Jones and Cohen, 2005), resulting from impaired prefrontal cortex (PFC) processing underlying executive functioning (Arnsten, 2009; Qin et al, 2009) and exhaustion of attentional resources (Sato et al, 2012). These disorders are characterized by aberrant corticosteroid signaling (Yehuda et al, 2001)
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