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Selective attention to emotional cues and emotion recognition in healthy subjects: the role of mineralocorticoid receptor stimulation

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Abstract

Rationale

Selective attention toward emotional cues and emotion recognition of facial expressions are important aspects of social cognition. Stress modulates social cognition through cortisol, which acts on glucocorticoid (GR) and mineralocorticoid receptors (MR) in the brain.

Objectives

We examined the role of MR activation on attentional bias toward emotional cues and on emotion recognition.

Methods

We included 40 healthy young women and 40 healthy young men (mean age 23.9 ± 3.3), who either received 0.4 mg of the MR agonist fludrocortisone or placebo. A dot-probe paradigm was used to test for attentional biases toward emotional cues (happy and sad faces). Moreover, we used a facial emotion recognition task to investigate the ability to recognize emotional valence (anger and sadness) from facial expression in four graded categories of emotional intensity (20, 30, 40, and 80 %).

Results

In the emotional dot-probe task, we found a main effect of treatment and a treatment × valence interaction. Post hoc analyses revealed an attentional bias away from sad faces after placebo intake and a shift in selective attention toward sad faces compared to placebo. We found no attentional bias toward happy faces after fludrocortisone or placebo intake. In the facial emotion recognition task, there was no main effect of treatment.

Conclusions

MR stimulation seems to be important in modulating quick, automatic emotional processing, i.e., a shift in selective attention toward negative emotional cues. Our results confirm and extend previous findings of MR function. However, we did not find an effect of MR stimulation on emotion recognition.

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References

  • Agarwal M, Coupry F, Philippe M (1977) Physiological activity and receptor binding of 9α fluorohydrocortisone. Biochem Biophys Res Commun 78:747–753

    Article  CAS  PubMed  Google Scholar 

  • Beck AT, Steer RA, Brown GK (1996) Manual for the beck depression inventory-II. San Antonio, TX: Psychological Corporation, 1, 82

  • Bogdan R, Williamson DE, Hariri AR (2012) Mineralocorticoid receptor Iso/Val (rs5522) genotype moderates the association between previous childhood emotional neglect and amygdala reactivity. Am J Psychiatr

  • Bradley MM, Codispoti M, Sabatinelli D, Lang PJ (2001) Emotion and motivation II: sex differences in picture processing. Emotion 1:300

    Article  CAS  PubMed  Google Scholar 

  • Breitberg A, Drevets WC, Wood SE, Mah L, Schulkin J, Sahakian BJ, Erickson K (2013) Hydrocortisone infusion exerts dose-and sex-dependent effects on attention to emotional stimuli. Brain Cogn 81:247–255

    Article  PubMed  Google Scholar 

  • Brinks V, van der Mark MH, de Kloet ER, Oitzl MS (2007) Differential MR/GR activation in mice results in emotional states beneficial or impairing for cognition. Neural plasticity 2007

  • Brinks V, Berger S, Gass P, De Kloet E, Oitzl M (2009) Mineralocorticoid receptors in control of emotional arousal and fear memory. Horm Behav 56:232–238

    Article  CAS  PubMed  Google Scholar 

  • Buckley TM, Mullen BC, Schatzberg AF (2007) The acute effects of a mineralocorticoid receptor (MR) agonist on nocturnal hypothalamic–adrenal–pituitary (HPA) axis activity in healthy controls. Psychoneuroendocrinology 32:859–864

    Article  CAS  PubMed  Google Scholar 

  • Cahill L (2006) Why sex matters for neuroscience. Nat Rev Neurosci 7:477–484

    Article  CAS  PubMed  Google Scholar 

  • Carr AR, Scully A, Webb M, Felmingham KL (2016) Gender differences in salivary alpha-amylase and attentional bias towards negative facial expressions following acute stress induction. Cognit Emot 30:315–324

    Article  Google Scholar 

  • De Kloet E (2013) Functional profile of the binary brain corticosteroid receptor system: mediating, multitasking, coordinating, integrating. Eur J Pharmacol 719:53–62

    Article  PubMed  Google Scholar 

  • de Kloet RE (2014) From receptor balance to rational glucocorticoid therapy. Endocrinology 155(8):2754–2769

    Article  PubMed  Google Scholar 

  • de Kloet ER, Oitzl MS, Joëls M (1999) Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 22:422–426

    Article  PubMed  Google Scholar 

  • Deckers JW, Lobbestael J, van Wingen GA, Kessels RP, Arntz A, Egger JI (2015) The influence of stress on social cognition in patients with borderline personality disorder. Psychoneuroendocrinology 52:119–129

    Article  PubMed  Google Scholar 

  • Duesenberg M, Weber J, Schulze L, Schaeuffele C, Roepke S, Hellmann-Regen J, Otte C, Wingenfeld K (2016) Does cortisol modulate emotion recognition and empathy? Psychoneuroendocrinology

  • Ebner NC, Riediger M, Lindenberger U (2010) FACES—a database of facial expressions in young, middle-aged, and older women and men: development and validation. Behav Res Methods 42:351–362

    Article  PubMed  Google Scholar 

  • Edwards S, Clow A, Evans P, Hucklebridge F (2001) Exploration of the awakening cortisol response in relation to diurnal cortisol secretory activity. Life Sci 68:2093–2103

    Article  CAS  PubMed  Google Scholar 

  • Faul F, Erdfelder E, Lang A-G, Buchner A (2007) G* Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39:175–191

    Article  PubMed  Google Scholar 

  • Gaffey AE, Wirth MM, Hoks RM, Jahn AL, Abercrombie HC (2014) Circulating cortisol levels after exogenous cortisol administration are higher in women using hormonal contraceptives: data from two preliminary studies. Stress 17:314–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groeneweg FL, Karst H, de Kloet ER, Joëls M (2012) Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling. Mol Cell Endocrinol 350:299–309

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann H, Kessler H, Eppel T, Rukavina S, Traue HC (2010) Expression intensity, gender and facial emotion recognition: women recognize only subtle facial emotions better than men. Acta Psychol 135:278–283

    Article  Google Scholar 

  • Joëls M, Karst H, DeRijk R, De Kloet ER (2008) The coming out of the brain mineralocorticoid receptor. Trends Neurosci 31:1–7

    Article  PubMed  Google Scholar 

  • Joëls M, Fernandez G, Roozendaal B (2011) Stress and emotional memory: a matter of timing. Trends Cogn Sci 15:280–288

    Article  PubMed  Google Scholar 

  • Joëls M, Sarabdjitsingh RA, Karst H (2012) Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes. Pharmacol Rev 64:901–938

    Article  PubMed  Google Scholar 

  • Joormann J, Gotlib IH (2007) Selective attention to emotional faces following recovery from depression. J Abnorm Psychol 116:80

    Article  PubMed  Google Scholar 

  • Karamouzis I, Berardelli R, Marinazzo E, D’Angelo V, Zinnà D, Minetto MA, Zichi C, Fussotto B, Giordano R, Ghigo E (2013) The acute effect of fludrocortisone on basal and hCRH-stimulated hypothalamic–pituitary–adrenal (HPA) axis in humans. Pituitary 16:378–385

    Article  CAS  PubMed  Google Scholar 

  • Kirschbaum C, Hellhammer DH (1989) Salivary cortisol in psychobiological research: an overview. Neuropsychobiology 22:150–169

    Article  CAS  PubMed  Google Scholar 

  • Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH (1999) Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom Med 61:154–162

    Article  CAS  PubMed  Google Scholar 

  • Klok MD, Alt SR, Irurzun Lafitte AJ, Turner JD, Lakke EA, Huitinga I, Muller CP, Zitman FG, de Kloet ER, Derijk RH (2011) Decreased expression of mineralocorticoid receptor mRNA and its splice variants in postmortem brain regions of patients with major depressive disorder. J Psychiatr Res 45(7):871–878

  • Lai M, Horsburgh K, Bae SE, Carter RN, Stenvers DJ, Fowler JH, Yau JL, Gomez‐Sanchez CE, Holmes MC, Kenyon CJ (2007) Forebrain mineralocorticoid receptor overexpression enhances memory, reduces anxiety and attenuates neuronal loss in cerebral ischaemia. Eur J Neurosci 25:1832–1842

    Article  PubMed  Google Scholar 

  • MacLeod C, Mathews A (1988) Anxiety and the allocation of attention to threat. Q J Exp Psychol 40:653–670

    Article  CAS  Google Scholar 

  • MacLeod C, Mathews A, Tata P (1986) Attentional bias in emotional disorders. J Abnorm Psychol 95:15

    Article  CAS  PubMed  Google Scholar 

  • McHugh RK, Behar E, Gutner CA, Geem D, Otto MW (2010) Cortisol, stress, and attentional bias toward threat. Anxiety Stress Coping 23:529–545

    Article  PubMed  Google Scholar 

  • Mitra R, Ferguson D, Sapolsky RM (2009) Mineralocorticoid receptor overexpression in basolateral amygdala reduces corticosterone secretion and anxiety. Biol Psychiatry 66:686–690

    Article  CAS  PubMed  Google Scholar 

  • Montagne B, Kessels RP, Frigerio E, de Haan EH, Perrett DI (2005) Sex differences in the perception of affective facial expressions: do men really lack emotional sensitivity? Cogn Process 6:136–141

    Article  PubMed  Google Scholar 

  • Oitzl MS, Champagne DL, van der Veen R, de Kloet ER (2010) Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci Biobehav Rev 34:853–866

    Article  CAS  PubMed  Google Scholar 

  • Otte C, Yassouridis A, Jahn H, Maass P, Stober N, Wiedemann K, Kellner M (2003) Mineralocorticoid receptor-mediated inhibition of the hypothalamic-pituitary-adrenal axis in aged humans. J Gerontol A Biol Sci Med Sci 58:B900–B905

    Article  PubMed  Google Scholar 

  • Putman P, Roelofs K (2011) Effects of single cortisol administrations on human affect reviewed: Coping with stress through adaptive regulation of automatic cognitive processing. Psychoneuroendocrinology 36:439–448

    Article  CAS  PubMed  Google Scholar 

  • Putman P, Hermans EJ, Koppeschaar H, Van Schijndel A, Van Honk J (2007) A single administration of cortisol acutely reduces preconscious attention for fear in anxious young men. Psychoneuroendocrinology 32:793–802

    Article  CAS  PubMed  Google Scholar 

  • Putman P, Hermans EJ, van Honk J (2010) Cortisol administration acutely reduces threat-selective spatial attention in healthy young men. Physiol Behav 99:294–300

    Article  CAS  PubMed  Google Scholar 

  • Ribot M, Polito A, Grassin-Delyle S, Annane D, Alvarez J-C (2013) Human plasma quantification of fludrocortisone using liquid chromatography coupled with atmospheric pressure chemical ionization mass spectrometry after low-dosage administration. Clin Chim Acta 420:109–113

    Article  CAS  PubMed  Google Scholar 

  • Rimmele U, Besedovsky L, Lange T, Born J (2013) Blocking mineralocorticoid receptors impairs, blocking glucocorticoid receptors enhances memory retrieval in humans. Neuropsychopharmacology 38:884–894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rimmele U, Besedovsky L, Lange T, Born J (2015) Emotional memory can be persistently weakened by suppressing cortisol during retrieval. Neurobiol Learn Mem 119:102–107

    Article  CAS  PubMed  Google Scholar 

  • Roelofs K, Bakvis P, Hermans EJ, van Pelt J, van Honk J (2007) The effects of social stress and cortisol responses on the preconscious selective attention to social threat. Biol Psychol 75:1–7

    Article  PubMed  Google Scholar 

  • Rolls ET (2015) Limbic systems for emotion and for memory, but no single limbic system. Cortex 62:119–157

    Article  PubMed  Google Scholar 

  • Rozeboom AM, Akil H, Seasholtz AF (2007) Mineralocorticoid receptor overexpression in forebrain decreases anxiety-like behavior and alters the stress response in mice. Proc Natl Acad Sci 104:4688–4693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandi C, Haller J (2015) Stress and the social brain: behavioural effects and neurobiological mechanisms. Nat Rev Neurosci 16:290–304

    Article  CAS  PubMed  Google Scholar 

  • Sheehan TP, Chambers RA, Russell DS (2004) Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Rev 46:71–117

    Article  PubMed  Google Scholar 

  • Singewald GM, Rjabokon A, Singewald N, Ebner K (2011) The modulatory role of the lateral septum on neuroendocrine and behavioral stress responses. Neuropsychopharmacology 36:793–804

    Article  PubMed  Google Scholar 

  • Steyer R, Schwenkmezger P, Notz P, Eid M (1997) MDBF–Mehrdimensionaler Befindlichkeitsfragebogen. Hogrefe, Göttingen

    Google Scholar 

  • Taylor VA, Ellenbogen MA, Washburn D, Joober R (2011) The effects of glucocorticoids on the inhibition of emotional information: a dose–response study. Biol Psychol 86:17–25

    Article  PubMed  Google Scholar 

  • ter Heegde F, De Rijk RH, Vinkers CH (2015) The brain mineralocorticoid receptor and stress resilience. Psychoneuroendocrinology 52:92–110

    Article  PubMed  Google Scholar 

  • Ter Horst J, Carobrez A, Van Der Mark M, De Kloet E, Oitzl M (2012) Sex differences in fear memory and extinction of mice with forebrain‐specific disruption of the mineralocorticoid receptor. Eur J Neurosci 36:3096–3102

    Article  PubMed  Google Scholar 

  • Thompson AE, Voyer D (2014) Sex differences in the ability to recognise non-verbal displays of emotion: a meta-analysis. Cognit Emot 28:1164–1195

    Article  Google Scholar 

  • Tottenham N, Tanaka JW, Leon AC, McCarry T, Nurse M, Hare TA, Marcus DJ, Westerlund A, Casey BJ, Nelson C (2009) The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Res 168:242–249

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsumura H, Shimada H (2012) Acutely elevated cortisol in response to stressor is associated with attentional bias toward depression-related stimuli but is not associated with attentional function. Appl Psychophysiol Biofeedback 37:19–29

    Article  PubMed  Google Scholar 

  • van Honk J, Tuiten A, van den Hout M, Koppeschaar H, Thijssen J, de Haan E, Verbaten R (1998) Baseline salivary cortisol levels and preconscious selective attention for threat: a pilot study. Psychoneuroendocrinology 23:741–747

    Article  PubMed  Google Scholar 

  • van Honk J, Tuiten A, van den Hout M, Koppeschaar H, Thijssen J, de Haan E, Verbaten R (2000) Conscious and preconscious selective attention to social threat: different neuroendocrine response patterns. Psychoneuroendocrinology 25:577–591

    Article  PubMed  Google Scholar 

  • Vogel S, Fernández G, Joëls M, Schwabe L (2016) Cognitive adaptation under stress: a case for the Mineralocorticoid Receptor. Trends Cogn Sci

  • Vogel S, Gerritsen L, van Oostrom I, Arias-Vásquez A, Rijpkema M, Joëls M, Franke B, Tendolkar I, Fernández G (2014) Linking genetic variants of the mineralocorticoid receptor and negative memory bias: interaction with prior life adversity. Psychoneuroendocrinology, 40, 181-190

  • Wingenfeld K, Kuehl LK, Janke K, Hinkelmann K, Dziobek I, Fleischer J, Otte C, Roepke S (2014) Enhanced emotional empathy after mineralocorticoid receptor stimulation in women with borderline personality disorder and healthy women. Neuropsychopharmacology 39:1799–1804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wittchen H-U, Fydrich T (1997) Strukturiertes Klinisches Interview für DSM-IV (SKID-I und SKID-II). Hogrefe

  • Zhou M, Kindt M, Joëls M, Krugers HJ (2011) Blocking mineralocorticoid receptors prior to retrieval reduces contextual fear memory in mice. PLoS One 6, e26220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We would like to thank all subjects for their participation in the present study.

Author contributions

Katharina Schultebraucks, Katja Wingenfeld, and Christian Otte developed study concept.

All authors contributed to the study design. Testing and data collection were performed by Katharina Schultebraucks, Antonia Domke and Lisa Lockenvitz. Katharina Schultebraucks performed data analysis and interpretation under the supervision of Katja Wingenfeld and Christian Otte. Katharina Schultebraucks drafted the manuscripts, and Katja Wingenfeld and Christian Otte provided critical revisions. Lars Schulze coded the facial emotion recognition task and Linn K. Kuehl and Christian E. Deuter coded the emotional dot-probe task. Moritz Duesenberg implemented the facial emotion recognition task. Julian Hellmann-Regen analyzed and interpreted the salivary cortisol data. All authors approved the final version of the manuscript for submission.

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Authors and Affiliations

  1. Department of Psychiatry and Psychotherapy, Charité Universitätsmedizin Berlin, Hindenburgdamm 30, 12203, Berlin, Germany

    Katharina Schultebraucks, Christian E. Deuter, Moritz Duesenberg, Julian Hellmann-Regen, Linn K. Kuehl, Christian Otte & Katja Wingenfeld

  2. Department of Clinical Psychology and Psychotherapy, Freie Universität Berlin, Berlin, Germany

    Lars Schulze & Antonia Domke

  3. Department of Psychology, Universität Potsdam, Potsdam, Germany

    Lisa Lockenvitz

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  1. Katharina Schultebraucks
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  2. Christian E. Deuter
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  3. Moritz Duesenberg
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  4. Lars Schulze
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  5. Julian Hellmann-Regen
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  6. Antonia Domke
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  8. Linn K. Kuehl
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  9. Christian Otte
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  10. Katja Wingenfeld
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Correspondence to Katharina Schultebraucks.

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All authors declared no conflicts of interest with respect to the authorship or the publication of this article.

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Schultebraucks, K., Deuter, C.E., Duesenberg, M. et al. Selective attention to emotional cues and emotion recognition in healthy subjects: the role of mineralocorticoid receptor stimulation. Psychopharmacology 233, 3405–3415 (2016). https://doi.org/10.1007/s00213-016-4380-0

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  • DOI: https://doi.org/10.1007/s00213-016-4380-0

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