Chemosignals of fear enhance cognitive performance in humans.

It is well documented across phyla that animals experiencing stress and fear produce chemical warning signals that can lead to behavioral, endocrinological, and immunological changes in the recipient animals of the same species. Humans distinguish between fear and other emotional chemosignals based on olfactory cues. Here, we study the effect of human fear chemosignals on the speed and accuracy of cognitive performance. In a double-blind experiment, female participants performed a word-association task while smelling one of the three types of olfactory stimuli: fear sweat, neutral sweat, and control odor carrier. We found that the participants exposed to the fear condition performed more accurately and yet with no sacrifice for speed on meaningful word conditions than those under either the neutral or the control condition. At the same time, they performed slower on tasks that contained ambiguous content. Possible factors that could introduce bias, such as individual differences due to anxiety, verbal skills, and perceived qualities of the smells, were ruled out. Our results demonstrate that human fear chemosignals enhance cognitive performances in the recipient. We suggest that this effect originates from learned associations, including greater cautiousness and concomitant changes in cognitive strategies.

[1]  R. Ader,et al.  Immune deviation following stress odor exposure: role of endogenous opioids , 2000, Journal of Neuroimmunology.

[2]  T. Scherer,et al.  Constraints for emotion specificity in fear and anger: the context counts. , 2001, Psychophysiology.

[3]  R. Cialdini,et al.  Alarm Pheromone in the Earthworm Lumbricus terrestris , 1968, Science.

[4]  M. McClintock,et al.  Menstrual Synchrony and Suppression , 1971, Nature.

[5]  R. Herz,et al.  Ambient odors associated to failure influence cognitive performance in children. , 1999, Developmental psychobiology.

[6]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[7]  David J. Klein,et al.  Psychophysiology of Emotion Across the Life Span , 1997, Annual Review of Gerontology and Geriatrics.

[8]  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.

[9]  W. Precht The synaptic organization of the brain G.M. Shepherd, Oxford University Press (1975). 364 pp., £3.80 (paperback) , 1976, Neuroscience.

[10]  H. Ehrlichman,et al.  Affect and memory: effects of pleasant and unpleasant odors on retrieval of happy and unhappy memories. , 1988, Journal of personality and social psychology.

[11]  M. Dean,et al.  Direct transfer of a lysosomal enzyme from lymphoid cells to deficient fibroblasts , 1981, Nature.

[12]  Peter J. Lang,et al.  Attention and Orienting : Sensory and Motivational Processes , 1997 .

[13]  J. Pardo,et al.  Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[14]  L. Kinnunen,et al.  Sustained human chemosignal unconsciously alters brain function , 2001, Neuroreport.

[15]  J. Desmond,et al.  Blind smell: brain activation induced by an undetected air-borne chemical. , 1999, Brain : a journal of neurology.

[16]  D. Nelson,et al.  The University of South Florida homograph norms , 1980 .

[17]  Donald E. Broadbent,et al.  Anxiety and Attentional Bias: State and Trait , 1988 .

[18]  M. Lowe,et al.  Human amygdala activation detected with echo-planar functional magnetic resonance imaging. , 1996, Neuroreport.

[19]  J. Gross,et al.  Emotion elicitation using films , 1995 .

[20]  K. Montgomery,et al.  The relation between fear induced by novel stimulation and exploratory behavior. , 1955, Journal of comparative and physiological psychology.

[21]  D. Thiessen,et al.  The effects of odors from stressed mice on conspecific behavior , 1991, Physiology & Behavior.

[22]  M. Liebowitz,et al.  Reaction time to threat stimuli in panic disorder and social phobia. , 1992, Behaviour research and therapy.

[23]  C. Snowdon,et al.  Demonstration and analysis of an alarm pheromone in mice. , 1972, Journal of comparative and physiological psychology.

[24]  Joel S. Warm,et al.  Effects of olfactory stimulation on performance and stress in a visual sustained attention task , 1991 .

[25]  Joseph E LeDoux,et al.  The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  W. J. Carr,et al.  Responses by young house mice (Mus musculus) to odors from stressed vs. nonstressed adult conspecifics , 1980 .

[27]  K. Mogg,et al.  Attentional Bias for Threatening Facial Expressions in Anxiety: Manipulation of Stimulus Duration , 1998 .

[28]  Denise Chen,et al.  Rapid mood change and human odors , 1999, Physiology & Behavior.

[29]  Y. M. Sheikh,et al.  Anthopleurine: a sea anemone alarm pheromone. , 1975, Science.

[30]  E. Abel Alarm substance emitted by rats in the forced-swim test is a low volatile pheromone , 1991, Physiology & Behavior.

[31]  Grant E Brown,et al.  Assessment of local predation risk: the role of subthreshold concentrations of chemical alarm cues , 2004 .

[32]  Duncan C. Blanchard,et al.  Risk assessment in animal models of anxiety , 1991 .

[33]  M. McClintock,et al.  Regulation of ovulation by human pheromones , 1998, Nature.

[34]  Tristram D. Wyatt Pheromones and Animal Behaviour: Pheromones and Animal Behaviour , 2003 .

[35]  D. Müller-Schwarze,et al.  Alert odor from skin gland in deer , 1984, Journal of Chemical Ecology.

[36]  Karl Grammer,et al.  The scent of fear. , 2002, Neuro endocrinology letters.

[37]  A. Richards,et al.  Word association norms for a set of threat/neutral homographs , 1992 .

[38]  J. Slangen,et al.  Animal Models in Psychopharmacology , 1991, APS: Advances in Pharmacological Sciences.

[39]  J. Bargh The ecology of automaticity: toward establishing the conditions needed to produce automatic processing effects. , 1992, The American journal of psychology.

[40]  Johan N Lundström,et al.  Psychological effects of subthreshold exposure to the putative human pheromone 4,16-androstadien-3-one , 2003, Hormones and Behavior.

[41]  G. Dodd,et al.  Unconscious odour conditioning in human subjects , 1983, Biological Psychology.

[42]  D. A. Thomas,et al.  Age of stress-produced odorants and the Kamin effect. , 1977, Behavioral biology.

[43]  Karen S. Quigley,et al.  Cardiac psychophysiology and autonomic space in humans: empirical perspectives and conceptual implications. , 1993, Psychological bulletin.

[44]  K. Frisch Über einen Schreckstoff der Fischhaut und seine biologische Bedeutung , 1942, Zeitschrift für vergleichende Physiologie.

[45]  J. Cacioppo,et al.  Handbook of psychophysiology (2nd ed.). , 2000 .

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

[47]  E. Wilson,et al.  The alarm-defence system of the ant Lasius alienus , 1969 .

[48]  J. Koolhaas,et al.  Individual Differences in Behavioural Reaction to a Changing Environment in Mice and Rats , 1987 .

[49]  K. Barnhart,et al.  Male Axillary Extracts Contain Pheromones that Affect Pulsatile Secretion of Luteinizing Hormone and Mood in Women Recipients1 , 2003, Biology of reproduction.

[50]  Steven M Platek,et al.  Cross-modal self-recognition: The role of visual, auditory, and olfactory primes , 2004, Consciousness and Cognition.

[51]  M. Bradley,et al.  Probing picture perception: activation and emotion. , 1996, Psychophysiology.

[52]  Keith Wesnes,et al.  AROMAS OF ROSEMARY AND LAVENDER ESSENTIAL OILS DIFFERENTIALLY AFFECT COGNITION AND MOOD IN HEALTHY ADULTS , 2003, The International journal of neuroscience.

[53]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[54]  J. Cacioppo,et al.  The psychophysiology of emotion. , 1993 .

[55]  W. Agosta Chemical Communication: The Language of Pheromones , 1992 .

[56]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[57]  Denise Chen,et al.  Human Olfactory Communication of Emotion , 2000, Perceptual and motor skills.

[58]  S. D. de Boer,et al.  Coping styles in animals: current status in behavior and stress-physiology , 1999, Neuroscience & Biobehavioral Reviews.

[59]  A. Richards,et al.  An Anxiety-Related Bias in Semantic Activation When Processing Threat/Neutral Homographs , 1992, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[60]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[61]  K. Montgomery,et al.  The relation between fear induced by novel stimulation and exploratory drive. , 1955 .

[62]  J. Cacioppo,et al.  Handbook Of Psychophysiology , 2019 .

[63]  David J. Anderson,et al.  A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila , 2004, Nature.

[64]  Wittko Francke Book Review: Chemical Communication. The Language of Pheromones. (Scientific American Library Series, Vol. 41.) By W. C. Agosta , 1994 .

[65]  M. Bradley,et al.  Motivated attention: Affect, activation, and action. , 1997 .

[66]  M. Dawson,et al.  The electrodermal system , 2007 .

[67]  T. Kikusui,et al.  Alarm pheromone enhances stress-induced hyperthermia in rats , 2001, Physiology & Behavior.

[68]  P. Dalton,et al.  Gender-specific induction of enhanced sensitivity to odors , 2002, Nature Neuroscience.

[69]  G. Preti,et al.  Analysis of human axillary volatiles: compounds of exogenous origin. , 1979, Journal of chromatography.

[70]  Gordon M. Shepherd,et al.  Olfactory cortex , 1998 .

[71]  Jean-Louis Millot,et al.  Ambient odors modulate visual attentional capture , 2003, Neuroscience Letters.

[72]  Jennifer A. Hobin,et al.  Auditory-Evoked Spike Firing in the Lateral Amygdala and Pavlovian Fear Conditioning Mnemonic Code or Fear Bias? , 2003, Neuron.

[73]  A. Ohman,et al.  Emotion drives attention: detecting the snake in the grass. , 2001, Journal of experimental psychology. General.

[74]  M. Powell Lawton,et al.  Annual Review of Gerontology and Geriatrics , 1988, Springer Berlin Heidelberg.

[75]  S. Paradiso,et al.  Book Review: Affective Neuroscience: The Foundations of Human and Animal Emotions , 2000 .

[76]  B. Gulyás,et al.  Smelling of Odorous Sex Hormone-like Compounds Causes Sex-Differentiated Hypothalamic Activations in Humans , 2001, Neuron.

[77]  J. Koolhaas,et al.  Routine Formation and Flexibility in Social and Non-Social Behaviour of Aggressive and Non-Aggressive Male Mice , 1990 .