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Research Article

Behavioral and neural correlates to multisensory detection of sick humans

View ORCID ProfileChristina Regenbogen, John Axelsson, View ORCID ProfileJulie Lasselin, Danja K. Porada, Tina Sundelin, Moa G. Peter, Mats Lekander, Johan N. Lundström, and Mats J. Olsson
PNAS first published May 22, 2017; https://doi.org/10.1073/pnas.1617357114
Christina Regenbogen
aDivision of Psychology, Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden;
bDepartment of Psychiatry, Psychotherapy and Psychosomatics, Medical School, Rheinisch-Westfälische Technische Hochschule Aachen, 52074 Aachen, Germany;
cJülich Aachen Research Alliance - BRAIN Institute 1: Structure Function Relationship, Jülich Aachen Research Alliance, 52425 Juelich, Germany;
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  • ORCID record for Christina Regenbogen
  • For correspondence: cregenbogen@ukaachen.de mats.j.olsson@ki.se
John Axelsson
aDivision of Psychology, Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden;
dStress Research Institute, Stockholm University, 106 91 Stockholm, Sweden;
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Julie Lasselin
aDivision of Psychology, Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden;
dStress Research Institute, Stockholm University, 106 91 Stockholm, Sweden;
eInstitute of Medical Psychology and Behavioral Immunobiology, Universitätsklinikum Essen, 45147 Essen, Germany;
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  • ORCID record for Julie Lasselin
Danja K. Porada
aDivision of Psychology, Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden;
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Tina Sundelin
aDivision of Psychology, Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden;
fDepartment of Psychology, Stockholm University, 106 91 Stockholm, Sweden;
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Moa G. Peter
aDivision of Psychology, Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden;
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Mats Lekander
aDivision of Psychology, Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden;
dStress Research Institute, Stockholm University, 106 91 Stockholm, Sweden;
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Johan N. Lundström
aDivision of Psychology, Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden;
gMonell Chemical Senses Center, Philadelphia, PA 19104;
hDepartment of Psychology, University of Pennsylvania, Philadelphia, PA 19104
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Mats J. Olsson
aDivision of Psychology, Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden;
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  • For correspondence: cregenbogen@ukaachen.de mats.j.olsson@ki.se
  1. Edited by Noam Sobel, Weizmann Institute, Rehovot, Israel, and accepted by Editorial Board Member Randolph Blake April 26, 2017 (received for review October 26, 2016)

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  • Olfactory and visual sickness
    - Jun 05, 2017
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Significance

In the perpetual race between evolving organisms and pathogens, the human immune system has evolved to reduce the harm of infections. As part of such a system, avoidance of contagious individuals would increase biological fitness. The present study shows that we can detect both facial and olfactory cues of sickness in others just hours after experimental activation of their immune system. The study further demonstrates that multisensory integration of these olfactory and visual sickness cues is a crucial mechanism for how we detect and socially evaluate sick individuals. Thus, by motivating the avoidance of sick conspecifics, olfactory–visual cues, both in isolation and integrated, may be important parts of circuits handling imminent threats of contagion.

Abstract

Throughout human evolution, infectious diseases have been a primary cause of death. Detection of subtle cues indicating sickness and avoidance of sick conspecifics would therefore be an adaptive way of coping with an environment fraught with pathogens. This study determines how humans perceive and integrate early cues of sickness in conspecifics sampled just hours after the induction of immune system activation, and the underlying neural mechanisms for this detection. In a double-blind placebo-controlled crossover design, the immune system in 22 sample donors was transiently activated with an endotoxin injection [lipopolysaccharide (LPS)]. Facial photographs and body odor samples were taken from the same donors when “sick” (LPS-injected) and when “healthy” (saline-injected) and subsequently were presented to a separate group of participants (n = 30) who rated their liking of the presented person during fMRI scanning. Faces were less socially desirable when sick, and sick body odors tended to lower liking of the faces. Sickness status presented by odor and facial photograph resulted in increased neural activation of odor- and face-perception networks, respectively. A superadditive effect of olfactory–visual integration of sickness cues was found in the intraparietal sulcus, which was functionally connected to core areas of multisensory integration in the superior temporal sulcus and orbitofrontal cortex. Taken together, the results outline a disease-avoidance model in which neural mechanisms involved in the detection of disease cues and multisensory integration are vital parts.

  • body odor
  • lipopolysaccharide
  • endotoxin
  • sickness cues
  • disease avoidance

Footnotes

  • ↵1To whom correspondence may be addressed. Email: cregenbogen{at}ukaachen.de or mats.j.olsson{at}ki.se.
  • ↵2J.N.L. and M.J.O. contributed equally to this work.

  • Author contributions: C.R., J.A., J.L., D.K.P., T.S., M.G.P., M.L., J.N.L., and M.J.O. designed research; C.R., D.K.P., M.G.P., J.N.L., and M.J.O. performed research; J.N.L. contributed new reagents/analytic tools; C.R. analyzed data; and C.R., J.A., J.L., T.S., M.L., J.N.L., and M.J.O. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. N.S. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1617357114/-/DCSupplemental.

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Multisensory sickness detection
Christina Regenbogen, John Axelsson, Julie Lasselin, Danja K. Porada, Tina Sundelin, Moa G. Peter, Mats Lekander, Johan N. Lundström, Mats J. Olsson
Proceedings of the National Academy of Sciences May 2017, 201617357; DOI: 10.1073/pnas.1617357114

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Multisensory sickness detection
Christina Regenbogen, John Axelsson, Julie Lasselin, Danja K. Porada, Tina Sundelin, Moa G. Peter, Mats Lekander, Johan N. Lundström, Mats J. Olsson
Proceedings of the National Academy of Sciences May 2017, 201617357; DOI: 10.1073/pnas.1617357114
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