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Time-Dependent Effects of Cortisol on Selective Attention and Emotional Interference: a Functional MRI Study

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Time-Dependent Effects of Cortisol on Selective Attention and Emotional Interference: a Functional MRI Study ORIGINAL RESEARCH ARTICLE published: 28 August 2012 INTEGRATIVE NEUROSCIENCE doi: 10.3389/fnint.2012.00066 Time-dependent effects of cortisol on selective attention and emotional interference: a functional MRI study MarloesJ.A.G.Henckens1,2*, Guido A. van Wingen 1,3, Marian Joëls 2 and Guillén Fernández 1,4 1 Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands 2 Department of Neuroscience and Pharmacology, Rudolf Magnus Institute, University Medical Center Utrecht, Utrecht, Netherlands 3 Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, Netherlands 4 Department of Cognitive Neuroscience, Radboud University Nijmegen Medical Centre, Nijmegen, Netherlands Edited by: Acute stress is known to induce a state of hypervigilance, allowing optimal detection Florin Dolcos, University of Illinois at of threats. Although one may benefit from sensitive sensory processing, it comes at Urbana-Champaign, USA the cost of unselective attention and increased distraction by irrelevant information. Reviewed by: Corticosteroids, released in response to stress, have been shown to profoundly influence Barry Setlow, University of Florida, USA brain function in a time-dependent manner, causing rapid non-genomic and slow genomic Hao Zhang, Duke University, USA effects. Here, we investigated how these time-dependent effects influence the neural Florin Dolcos, University of Illinois at mechanisms underlying selective attention and the inhibition of emotional distracters Urbana-Champaign, USA in humans. Implementing a randomized, double-blind, placebo-controlled design, 65 Jessica Payne, University of Notre Dame, USA young healthy men received 10 mg hydrocortisone either 60 min (rapid effects) or *Correspondence: 270 min (slow effects), or placebo prior to an emotional distraction task, consisting Marloes J. A. G. Henckens, Centre of color-naming of either neutral or aversive words. Overall, participants responded for Cognitive Neuroimaging, slower to aversive compared to neutral words, indicating emotional interference with Donders Institute for Brain, selective attention. Importantly, the rapid effects of corticosteroids increased emotional Cognition and Behaviour, Radboud University Nijmegen, PO Box 9101, interference, which was associated with reduced amygdala inhibition to aversive words. 6500 HB Nijmegen, Netherlands. Moreover, they induced enhanced amygdala connectivity with frontoparietal brain regions, e-mail: [email protected] 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. Keywords: corticosteroids, emotional interference, attention, functional MRI, amygdala, prefrontal cortex, cuneus, insula INTRODUCTION et al., 2000; Braunstein-Bercovitz et al., 2001; Aston-Jones and Stress has profound influence on the brain’s attentional resources. Cohen, 2005), resulting from impaired prefrontal cortex (PFC) When exposed to an acutely stressful situation, the brain shifts processing underlying executive functioning (Arnsten, 2009; Qin into a mode of hypervigilant processing in which the detection et al., 2009) and exhaustion of attentional resources (Sato et al., and assessment of potential threats is optimized by prioritized 2012). It might cumulate in stress-related disorders such as sensory processing (de Kloet et al., 2005; van Marle et al., 2009), depression and post-traumatic stress disorder (PTSD), which are and the amygdala, key modulator of vigilance and emotional pro- characterized by an attentional bias toward negative emotional cessing in the brain (Phelps and Ledoux, 2005), is activated (van information (Williams et al., 1996). Therefore, normalization Marle et al., 2009). This surge in vigilance in immediate response of attentional processing some time after the stressful event is to stress is thought to be mediated by the central release of nore- very important for well-being. Notably, these disorders are char- pinephrine (NE) by tonic activation of the locus coeruleus (LC) acterized by aberrant corticosteroid signaling (Yehuda et al., (Aston-Jones and Cohen, 2005; Valentino and Van Bockstaele, 2001). 2008; Cousijn et al., 2010). This state of hypervigilance is highly Corticosteroids, released in response to stress as the end- adaptive and enhances chances of survival during stressful situa- product of the hypothalamic-pituitary-adrenal (HPA) axis, are tions, but it comes at the cost of specificity (van Marle et al., 2009), well-known modulators of human cognition. The hormones impaired selective attention (Tanji and Hoshi, 2008; Henderson exert their actions upon binding of the mineralocorticoid et al., 2012) and increased susceptibility to distraction (Skosnik (MR) and glucocorticoid receptor (GR), which are abundantly Frontiers in Integrative Neuroscience www.frontiersin.org August 2012 | Volume 6 | Article 66 | 1 Henckens et al. Corticosteroid modulation of attentive processing expressed in the brain (Sapolsky et al., 1983; Reul and de Kloet, MATERIALS AND METHODS 1985; de Kloet, 1991). Recent research in rodents has indicated PARTICIPANTS that corticosteroid-binding can induce both rapid non-genomic Seventy-two young (age range 18–29, median 21), right-handed, and slow genomic effects by acting on receptors that are respec- Dutch speaking, healthy male volunteers gave written informed tively located in the plasma membrane and in the nucleus (Di consent to participate in the study. Women were excluded from et al., 2003; Karst et al., 2005; Wiegert et al., 2005). These distinct participation, since previous research has indicated that women temporal pathways are thought to serve different functions (Joels respond differently to hydrocortisone than men, both in behav- et al., 2006, 2011). The rapid actions of corticosteroids on the one ior (Andreano and Cahill, 2006; Bohnke et al., 2010)andbrain hand, have been suggested to work in concert with (and amplify) activation (Stark et al., 2006; Merz et al., 2010). Moreover, the effects of catecholamines (Roozendaal et al., 2006; Joels and their response to hydrocortisone is modulated by oral contra- Baram, 2009) to optimize rapid adaptive behavior by relocat- ceptive use and varies over the menstrual cycle (Merz et al., ing neural resources away from higher-order cognitive processing 2011). Therefore, in order to reduce variance we here recruited regions in the PFC to the limbic structures (Diamond et al., the group with the most stable response to hydrocortisone. 2007). Therefore, they might boost the effects of catecholamines Furthermore, individuals who met any of the following criteria on attentional processing, increasing emotional interference. The were excluded from participation: history of head injury, auto- slow corticosteroid-induced genomic cascade is on the other hand nomic failure, history of or current psychiatric, neurological, or thought to be responsible for the regulation of the stress response endocrine disorders, current periodontitis, acute inflammatory and the restoration of homeostasis in the aftermath of stress (de disease, acute peptic or duodenal ulcers, regular use of corti- Kloet et al., 2005; Henckens et al., 2010, 2011c).Thereby, the slow costeroids, treatment with psychotropic medications, narcotics, corticosteroid effects might contribute to the normalization of beta-blockers, steroids, or any other medication that affects cen- attentional processing in the aftermath of stress. However, these tral nervous system or endocrine systems, medical illness within time-dependent effects of corticosteroids on the neural substrates the three weeks prior to testing, self reported mental or sub- of selective attention have never been tested. stance use disorder, daily tobacco or alcohol use (or experienced Here, we set out to investigate the time-dependent effects of inconvenience in refraining from these activities for three days), corticosteroids on the neural correlates of selective attentional exercising at the professional level, regular night shift work, or processing. In a randomized, double-blind, placebo-controlled current stressful episode or major life event. Four participants design, 65 young healthy men received 10 mg hydrocortisone were excluded from analyses because of unreliable cortisol manip- either 60 min (to target the rapid corticosteroid effects) or ulation [abnormal basal cortisol levels (1 × placebo) or no 270 min (slow corticosteroid effects), or placebo prior to func- elevation in salivary cortisol level in response to CORT intake tional MRI scanning. Selective attention was assessed by means (2 × rapid CORT, 1 × slow CORT)], and another three partic- of an emotional distraction task, in which participants were ipants because of insufficient task performance (based on out- asked to identify the font color of neutral and highly aversive lier analyses (>3 SD below average performance; 2
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