CoChat
Sign Up
Cited by 21Olfactory and Sensory Function StudiesPsychology of Moral and Emotional JudgmentFace Recognition and Perception

The DOI matches its Crossref record; 7 of the 7 references it cites were found in a registry or an index.

Human chemosignals of disgust facilitate food judgment

Open access
Zheng, Yan, You, Yuqi, Farias, Ana R., Simon, Jessica, Semin, Gün R., Smeets, Monique A., Li, Wen·2018·Scientific Reports
DOI 10.1038/s41598-018-35132-wPMC PMC6242886
Open this paper in CoChat — free accountOpen PDF

Abstract

Choosing food is not a trivial decision that people need to make daily, which is often subject to social influences. Here, we studied a human homolog of social transmission of food preference (STFP) as observed in rodents and other animals via chemosignals of body secretions. Human social chemosignals (sweat) produced during a disgust or neutral state among a group of donors were presented to participants undergoing a 2-alternative-forced-choice food healthiness judgment task during functional magnetic resonance imaging (fMRI). Response speed and two key signal detection indices— d’ (discrimination sensitivity) and β (response bias)—converged to indicate that social chemosignals of disgust facilitated food healthiness decisions, in contrast to primary disgust elicitors (disgust odors) that impaired the judgment. fMRI analyses (disgust vs. neutral sweat) revealed that the fusiform face area (FFA), amygdala, and orbitofrontal cortex (OFC) were engaged in processing social chemosignals of disgust during food judgment. Importantly, a double contrast of social signaling across modalities (olfactory vs. visual—facial expressions) indicated that the FFA and OFC exhibited preferential response to social chemosignals of disgust. Together, our findings provide initial evidence for human STFP, where social chemosignals are incorporated into food decisions by engaging social and emotional areas of the brain.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41598-018-35132-w

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Show all 7 references

Research works printed but not linked: 52

  1. Carels, R. A., Harper, J. & Konrad, K. Qualitative perceptions and caloric estimations of healthy and unhealthy foods by behavioral weight loss participants. Appetite 46, 199–206 (2006). · DOI
  2. Provencher, V., Polivy, J. & Herman, C. P. Perceived healthiness of food. If it’s healthy, you can eat more! Appetite 52, 340–344 (2009). · DOI · Paper page
  3. Tirindelli, R., Dibattista, M., Pifferi, S. & Menini, A. From pheromones to behavior. Physiological reviews 89, 921–956 (2009). · DOI
  4. Touhara, K. & Vosshall, L. B. Sensing odorants and pheromones with chemosensory receptors. Annual review of physiology 71 (2009). · DOI
  5. Katz, L. B. & Dill, L. M. The scent of death: chemosensory assessment of predation risk by animals. Ecoscience 5, 361–394 (1998). · DOI
  6. Galef, B. G. Jr, Mason, J. R., Preti, G. & Bean, N. J. Carbon disulfide: a semiochemical mediating socially-induced diet choice in rats. Physiology & Behavior 42, 119–124 (1988). · DOI
  7. Munger, S. D. et al. An olfactory subsystem that detects carbon disulfide and mediates food-related social learning. Current biology 20, 1438–1444 (2010). · DOI
  8. Shepherd, G. M. Neurogastronomy: how the brain creates flavor and why it matters (Columbia University Press, 2011). · DOI
  9. Maier, J. X., Blankenship, M. L., Barry, N. C., Richards, S. E. & Katz, D. B. Stability and flexibility of the message carried by semiochemical stimuli, as revealed by devaluation of carbon disulfide followed by social transmission of food preference. Behavioral neuroscience 128, 413 (2014). · DOI
  10. Bushdid, C., Magnasco, M. O., Vosshall, L. B. & Keller, A. Humans can discriminate more than 1 trillion olfactory stimuli. Science 343, 1370–1372 (2014). · DOI
  11. Laska, M., Genzel, D. & Wieser, A. The number of functional olfactory receptor genes and the relative size of olfactory brain structures are poor predictors of olfactory discrimination performance with enantiomers. Chemical senses 30, 171–175 (2005). · DOI
  12. Laska, M., Seibt, A. & Weber, A. ‘Microsmatic’ primates revisited: olfactory sensitivity in the squirrel monkey. Chemical Senses 25, 47–53 (2000). · DOI
  13. Hall, J. A., Coats, E. J. & LeBeau, L. S. Nonverbal behavior and the vertical dimension of social relations: a meta-analysis. Psychological bulletin 131, 898 (2005). · DOI
  14. App, B., McIntosh, D. N., Reed, C. L. & Hertenstein, M. J. Nonverbal channel use in communication of emotion: How may depend on why. Emotion 11, 603 (2011). · DOI
  15. Ekman, P., Friesen, W. V., Osullivan, M. & Scherer, K. Relative Importance of Face, Body, and Speech in Judgments of Personality and Affect. Journal of Personality and Social Psychology 38, 270–277, https://doi.org/10.1037//0022-3514.38.2.270 (1980). · DOI
  16. Semin, G. R. & De Groot, J. H. B. The chemical bases of human sociality. Trends in Cognitive Sciences 17, 427–429 (2013). · DOI
  17. Lundström, J. N. & Olsson, M. J. In Vitamins & Hormones Vol. 83, 1–23 (Elsevier, 2010). · DOI
  18. Frumin, I. et al. A social chemosignaling function for human handshaking. Elife 4, e05154 (2015). · DOI
  19. Olsson, M. J. et al. The scent of disease: human body odor contains an early chemosensory cue of sickness. Psychological science 25, 817–823 (2014). · DOI · Paper page
  20. Chen, D. & Haviland-Jones, J. Human olfactory communication of emotion. Perceptual and motor skills 91, 771–781 (2000). · DOI · Paper page
  21. Li, W. Learning to smell danger: acquired associative representation of threat in the olfactory cortex. Frontiers in behavioral neuroscience 8, 98 (2014).
  22. Mujica-Parodi, L. R. et al. Chemosensory cues to conspecific emotional stress activate amygdala in humans. PLoS One 4, e6415 (2009). · DOI
  23. Prehn, A., Ohrt, A., Sojka, B., Ferstl, R. & Pause, B. M. Chemosensory anxiety signals augment the startle reflex in humans. Neuroscience letters 394, 127–130 (2006). · DOI
  24. Zhou, W. & Chen, D. Fear-related chemosignals modulate recognition of fear in ambiguous facial expressions. Psychological science 20, 177–183 (2009). · DOI · Paper page
  25. Regenbogen, C. et al. Behavioral and neural correlates to multisensory detection of sick humans. Proceedings of the National Academy of Sciences 114, 6400–6405 (2017). · DOI
  26. Rozin, P. & Fallon, A. E. A perspective on disgust. Psychol Rev 94, 23–41 (1987). · DOI
  27. Chapman, H. A. & Anderson, A. K. Understanding disgust. Ann NY Acad Sci 1251, 62–76, https://doi.org/10.1111/j.1749-6632.2011.06369.x (2012). · DOI
  28. Fusar-Poli, P. et al. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 34, 418–432 (2009). · DOI · Paper page
  29. Sabatinelli, D. et al. Emotional perception: meta-analyses of face and natural scene processing. Neuroimage 54, 2524–2533, https://doi.org/10.1016/j.neuroimage.2010.10.011 (2011). · DOI
  30. Allison, T., Puce, A. & McCarthy, G. Social perception from visual cues: role of the STS region. Trends Cogn Sci 4, 267–278 (2000). · DOI · Paper page
  31. Lundstrom, J. N., Boyle, J. A., Zatorre, R. J. & Jones-Gotman, M. Functional neuronal processing of body odors differs from that of similar common odors. Cereb Cortex 18, 1466–1474, https://doi.org/10.1093/cercor/bhm178 (2008). · DOI · Paper page
  32. Prehn-Kristensen, A. et al. Induction of empathy by the smell of anxiety. PLoS One 4, e5987, https://doi.org/10.1371/journal.pone.0005987 (2009). · DOI
  33. Pause, B. M. Processing of Body Odor Signals by the Human Brain. Chemosens Percept 5, 55–63, https://doi.org/10.1007/s12078-011-9108-2 (2012). · DOI · Paper page
  34. Zhou, W. & Chen, D. Encoding human sexual chemosensory cues in the orbitofrontal and fusiform cortices. J Neurosci 28, 14416–14421, https://doi.org/10.1523/JNEUROSCI.3148-08.2008 (2008). · DOI
  35. Konkle, T., Brady, T. F., Alvarez, G. A. & Oliva, A. Conceptual distinctiveness supports detailed visual long-term memory for real-world objects. J Exp Psychol Gen 139, 558–578, https://doi.org/10.1037/a0019165 (2010). · DOI
  36. Willenbockel, V. et al. Controlling low-level image properties: The SHINE toolbox. Behav Res Methods 42, 671–684, https://doi.org/10.3758/Brm.42.3.671 (2010). · DOI · Paper page
  37. Lundqvist, D., Flykt, A. & Öhman, A. The Karolinska Directed Emotional Faces (1998). · DOI
  38. Doty, R. L., Orndorff, M. M., Leyden, J. & Kligman, A. Communication of gender from human axillary odors: relationship to perceived intensity and hedonicity. Behavioral biology 23, 373–380 (1978). · DOI
  39. Lorig, T. S., Elmes, D. G., Zald, D. H. & Pardo, J. V. A computer-controlled olfactometer for fMRI and electrophysiological studies of olfaction. Behav Res Methods Instrum Comput 31, 370–375 (1999). · DOI
  40. Novak, L. R., Gitelman, D. R., Schuyler, B. & Li, W. Olfactory-visual integration facilitates perception of subthreshold negative emotion. Neuropsychologia 77, 288–297, https://doi.org/10.1016/j.neuropsychologia.2015.09.005 (2015). · DOI
  41. Forscher, E. C. & Li, W. Hemispheric asymmetry and visuo-olfactory integration in perceiving subthreshold (micro) fearful expressions. J Neurosci 32, 2159–2165, https://doi.org/10.1523/JNEUROSCI.5094-11.2012 (2012). · DOI
  42. Krusemark, E. A. & Li, W. From early sensory specialization to later perceptual generalization: dynamic temporal progression in perceiving individual threats. J Neurosci 33, 587–594, https://doi.org/10.1523/JNEUROSCI.1379-12.2013 (2013). · DOI
  43. Krusemark, E. A. & Li, W. Do all threats work the same way? Divergent effects of fear and disgust on sensory perception and attention. J Neurosci 31 3429–3434 31/9/3429 (2011). · DOI
  44. Ashburner, J. A fast diffeomorphic image registration algorithm. Neuroimage 38, 95–113, https://doi.org/10.1016/j.neuroimage.2007.07.007 (2007). · DOI · Paper page
  45. Rorden, C. & Brett, M. Stereotaxic display of brain lesions. Behav Neurol 12, 191–200 (2000). · DOI
  46. Mai, J. K., Assheuer, J. & Paxinos, G. Atlas of the Human Brain (Thieme, 1997).
  47. Seubert, J., Freiherr, J., Djordjevic, J. & Lundstrom, J. N. Statistical localization of human olfactory cortex. Neuroimage 66, 333–342, https://doi.org/10.1016/j.neuroimage.2012.10.030 (2013). · DOI
  48. Galef, B. G. Jr., Wigmore, S. W. & Kennett, D. J. A failure to find socially mediated taste aversion learning in Norway rats (R. norvegicus). J Comp Psychol 97, 358–363 (1983). · DOI
  49. Carmichael, S. T., Clugnet, M. C. & Price, J. L. Central olfactory connections in the macaque monkey. Journal of Comparative Neurology 346, 403–434 (1994). · DOI
  50. Berridge, K. C. & Kringelbach, M. L. Neuroscience of affect: brain mechanisms of pleasure and displeasure. Curr Opin Neurobiol 23, 294–303, https://doi.org/10.1016/j.conb.2013.01.017 (2013). · DOI
  51. LeDoux, J. E. Emotion: clues from the brain. Annu Rev Psychol 46, 209–235 (1995). · DOI · Paper page
  52. von Kriegstein, K., Kleinschmidt, A., Sterzer, P. & Giraud, A. L. Interaction of face and voice areas during speaker recognition. J Cogn Neurosci 17, 367–376, https://doi.org/10.1162/0898929053279577 (2005). · DOI

Cited by

Sorted by citations

See all 21

Metadata

Authors
Zheng, Y., You, Y., Farias, A. R., Simon, J., Semin, G. R., Smeets, M. A., & Li, W.
Affiliations
  • Florida State University (US)
  • Universidade do Porto (PT)
  • Utrecht University (NL)
Corresponding author
Li, Wen
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2018-11-19
Volume
8
Issue
1
Pages
17006-17006
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-018-35132-w
PMC
PMC6242886
OpenAlex
W2901725456
Cited by
21
References
7
Citations by year
2025: 2 · 2023: 7 · 2022: 2 · 2021: 4 · 2020: 6
FWCI
1.62
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
  • Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, cc-by-nc)
  • Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, cc-by)
Funders
U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (R01MH093413)
Topics
  • Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Psychology of Moral and Emotional Judgment
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
Keywords
sweat, disgust, social transmission of food preference, olfactory cues, fusiform face area, amygdala, orbitofrontal cortex, food choice, social influences on eating
MeSH terms
Disgust, Adolescent, Adult, Amygdala, Brain, Brain Mapping, Emotions, Facial Expression, Female, Food Preferences, Humans, Judgment, Magnetic Resonance Imaging, Male, Reaction Time, Sweat, Prefrontal Cortex, Pheromones, Human, Young Adult

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review