The human body odor compound androstadienone increases neural conflict coupled to higher behavioral costs during an emotional Stroop task

&NA; The androgen derivative androstadienone (AND) is a substance found in human sweat and thus may act as human chemosignal. With the current experiment, we aimed to explore in which way AND affects interference processing during an emotional Stroop task which used human faces as target and emotional words as distractor stimuli. This was complemented by functional magnetic resonance imaging (fMRI) to unravel the neural mechanism of AND‐action. Based on previous accounts we expected AND to increase neural activation in areas commonly implicated in evaluation of emotional face processing and to change neural activation in brain regions linked to interference processing. For this aim, a total of 80 healthy individuals (oral contraceptive users, luteal women, men) were tested twice on two consecutive days with an emotional Stroop task using fMRI. Our results suggest that AND increases interference processing in brain areas that are heavily recruited during emotional conflict. At the same time, correlation analyses revealed that this neural interference processing was paralleled by higher behavioral costs (response times) with higher interference related brain activation under AND. Furthermore, AND elicited higher activation in regions implicated in emotional face processing including right fusiform gyrus, inferior frontal gyrus and dorsomedial cortex. In this connection, neural activation was not coupled to behavioral outcome. Furthermore, despite previous accounts of increased hypothalamic activation under AND, we were not able to replicate this finding and discuss possible reasons for this discrepancy. To conclude, AND increased interference processing in regions heavily recruited during emotional conflict which was coupled to higher costs in resolving emotional conflicts with stronger interference‐related brain activation under AND. At the moment it remains unclear whether these effects are due to changes in conflict detection or resolution. However, evidence most consistently suggests that AND does not draw attention to the most potent socio‐emotional information (human faces) but rather highlights representations of emotional words.

[1]  P. Pauli,et al.  Androstadienone in Motor Reactions of Men and Women toward Angry Faces , 2012, Perceptual and motor skills.

[2]  Ivanka Savic,et al.  Brain response to putative pheromones in lesbian women. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Susan C. Roberts,et al.  Evidence that androstadienone, a putative human chemosignal, modulates women’s attributions of men’s attractiveness , 2008, Hormones and Behavior.

[4]  R. Reitan Trail Making Test: Manual for Administration and Scoring , 1992 .

[5]  Monique A M Smeets,et al.  Chemosignals Communicate Human Emotions , 2012, Psychological science.

[6]  L. Monti-Bloch,et al.  Behavioral and electrophysiological effects of androstadienone, a human pheromone , 2000, Psychoneuroendocrinology.

[7]  S. Frühholz,et al.  Perceiving emotional expressions in others: Activation likelihood estimation meta-analyses of explicit evaluation, passive perception and incidental perception of emotions , 2016, Neuroscience & Biobehavioral Reviews.

[8]  D. Veltman,et al.  Heterosexual Men and Women Both Show a Hypothalamic Response to the Chemo-Signal Androstadienone , 2012, PloS one.

[9]  David W. Kern,et al.  A human chemosignal modulates frontolimbic activity and connectivity in response to emotional stimuli , 2017, Psychoneuroendocrinology.

[10]  T. Wyatt Fifty years of pheromones , 2009, Nature.

[11]  Tobias Egner,et al.  The neural correlates and functional integration of cognitive control in a Stroop task , 2005, NeuroImage.

[12]  T. Wyatt,et al.  The search for human pheromones: the lost decades and the necessity of returning to first principles , 2015, Proceedings of the Royal Society B: Biological Sciences.

[13]  P. Karlson,et al.  ‘Pheromones’: a New Term for a Class of Biologically Active Substances , 1959, Nature.

[14]  M. Gingnell,et al.  Menstrual cycle influence on cognitive function and emotion processing—from a reproductive perspective , 2014, Front. Neurosci..

[15]  E. Kandel,et al.  Resolving Emotional Conflict: A Role for the Rostral Anterior Cingulate Cortex in Modulating Activity in the Amygdala , 2006, Neuron.

[16]  M. Bensafi,et al.  Sniffing human sex-steroid derived compounds modulates mood, memory and autonomic nervous system function in specific behavioral contexts , 2003, Behavioural Brain Research.

[17]  K. T. Holland,et al.  Comparison of 16-Androstene steroid concentrations in sterile apocrine sweat and axillary secretions: Interconversions of 16-Androstenes by the axillary microflora—a mechanism for axillary odour production in man? , 1994, Journal of Steroid Biochemistry and Molecular Biology.

[18]  A. Mallet,et al.  Simultaneous quantification of five odorous steroids (16-androstenes) in the axillary hair of men. , 1988, Journal of steroid biochemistry.

[19]  M. McClintock,et al.  Putative human pheromone androstadienone attunes the mind specifically to emotional information , 2009, Hormones and Behavior.

[20]  U. Castiello,et al.  Subliminally Perceived Odours Modulate Female Intrasexual Competition: An Eye Movement Study , 2012, PloS one.

[21]  S. Delplanque,et al.  Androstadienone’s influence on the perception of facial and vocal attractiveness is not sex specific , 2016, Psychoneuroendocrinology.

[22]  Jessica Freiherr,et al.  The 40-item Monell Extended Sniffin’ Sticks Identification Test (MONEX-40) , 2012, Journal of Neuroscience Methods.

[23]  U. Habel,et al.  Conflict adaptation in emotional task underlies the amplification of target. , 2014, Emotion.

[24]  M. McClintock,et al.  Psychological State and Mood Effects of Steroidal Chemosignals in Women and Men , 2000, Hormones and Behavior.

[25]  C. Carter,et al.  Anterior cingulate cortex and conflict detection: An update of theory and data , 2007, Cognitive, affective & behavioral neuroscience.

[26]  T. Hummel,et al.  Individual differences in sensitivity to the odor of 4,16-androstadien-3-one. , 2003, Chemical senses.

[27]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[28]  M. Wiesmann,et al.  Smelling chemosensory signals of males in anxious versus nonanxious condition increases state anxiety of female subjects. , 2011, Chemical senses.

[29]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[30]  T. Egner,et al.  Dissociable neural systems resolve conflict from emotional versus nonemotional distracters. , 2008, Cerebral cortex.

[31]  F. Petermann Frankfurter Aufmerksamkeits-­Inventar 2 (FAIR-2) , 2011 .

[32]  R. Thornhill,et al.  Original Articles Hormonal correlates of women's mid-cycle preference for the scent of symmetry , 2008 .

[33]  Anette Kersting,et al.  Women's Greater Ability to Perceive Happy Facial Emotion Automatically: Gender Differences in Affective Priming , 2012, PloS one.

[34]  M L Phillips,et al.  Gender Differences in the Sensitivity to Negative Stimuli: Cross-Modal Affective Priming Study☆ , 2013, European Psychiatry.

[35]  S. Eickhoff,et al.  Neuroscience and Biobehavioral Reviews Three Key Regions for Supervisory Attentional Control: Evidence from Neuroimaging Meta-analyses , 2022 .

[36]  B. Derntl,et al.  The human body odor compound androstadienone leads to anger-dependent effects in an emotional Stroop but not dot-probe task using human faces , 2017, PloS one.

[37]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[38]  M. McClintock,et al.  Context-dependent effects of steroid chemosignals on human physiology and mood , 2001, Physiology & Behavior.

[39]  T. Kikusui,et al.  Alarm pheromones with different functions are released from different regions of the body surface of male rats. , 2004, Chemical senses.

[40]  D. Weissman,et al.  Congruency sequence effects are driven by previous-trial congruency, not previous-trial response conflict , 2013, Front. Psychol..

[41]  Colin M. Macleod Half a century of research on the Stroop effect: an integrative review. , 1991, Psychological bulletin.

[42]  B. Turetsky,et al.  The influence of androstadienone during psychosocial stress is modulated by gender, trait anxiety and subjective stress: An fMRI study , 2016, Psychoneuroendocrinology.

[43]  T. Egner,et al.  Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information , 2005, Nature Neuroscience.

[44]  Ute Habel,et al.  Brain Circuitries Involved in Semantic Interference by Demands of Emotional and Non-Emotional Distractors , 2012, PloS one.

[45]  Yang Yang,et al.  Neural Systems Underlying Emotional and Non-emotional Interference Processing: An ALE Meta-Analysis of Functional Neuroimaging Studies , 2016, Front. Behav. Neurosci..

[46]  Jessica Freiherr,et al.  You Smell Dangerous: Communicating Fight Responses Through Human Chemosignals of Aggression. , 2016, Chemical senses.

[47]  B. Derntl,et al.  Bayesian informed evidence against modulation of androstadienone-effects by genotypic receptor variants and participant sex: A study assessing Stroop interference control, mood and olfaction , 2018, Hormones and Behavior.

[48]  M. Bushnell,et al.  The effects of the steroid androstadienone and pleasant odorants on the mood and pain perception of men and women , 2007, European journal of pain.

[49]  Ivanka Savic,et al.  Brain response to putative pheromones in homosexual men. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[50]  T. Kikusui,et al.  Alarm pheromone increases defensive and risk assessment behaviors in male rats , 2006, Physiology & Behavior.

[51]  Natalie C. Ebner,et al.  FACES—A database of facial expressions in young, middle-aged, and older women and men: Development and validation , 2010, Behavior research methods.

[52]  Jessica Freiherr,et al.  The Influence of Menstrual Cycle and Androstadienone on Female Stress Reactions: An fMRI Study , 2016, Front. Hum. Neurosci..