Human Tears Contain a Chemosignal
Abstract
Emotional tearing is a poorly understood behavior that is considered uniquely human. In mice, tears serve as a chemosignal. We therefore hypothesized that human tears may similarly serve a chemosignaling function. We found that merely sniffing negative-emotion–related odorless tears obtained from women donors induced reductions in sexual appeal attributed by men to pictures of women’s faces. Moreover, after sniffing such tears, men experienced reduced self-rated sexual arousal, reduced physiological measures of arousal, and reduced levels of testosterone. Finally, functional magnetic resonance imaging revealed that sniffing women’s tears selectively reduced activity in brain substrates of sexual arousal in men.
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Supplementary Material
References and Notes
1
C. Darwin, The Expression of the Emotions in Man and Animals, with an introduction, afterword, and commentaries by Paul Ekman (Oxford Univ. Press, New York, 1872).
2
Chapman H. A., Kim D. A., Susskind J. M., Anderson A. K., In bad taste: Evidence for the oral origins of moral disgust. Science 323, 1222 (2009).
3
Montague A., Natural selection and the origin and evolution of weeping in man. Science 130, 1572 (1959).
4
Provine R. R., Krosnowski K. A., Brocato N. W., Tearing: Breakthrough in human emotional signaling. Evol. Psychol. 7, 78 (2009).
5
Vingerhoets A., Cornelius R. R., Van Heck G. L., Becht M. C., Adult crying: A model and review of the literature. Rev. Gen. Psychol. 4, 354 (2000).
6
Hendriks M. C., Croon M. A., Vingerhoets A. J., Social reactions to adult crying: The help-soliciting function of tears. J. Soc. Psychol. 148, 22 (2008).
7
W. H. Frey, M. Langseth, Crying: The Mystery of Tears (Winston Press, Minneapolis, MN, 1985).
8
N. H. Frijda, The Emotions (Cambridge Univ. Press, 1986).
9
Van Haeringen N. J., Clinical biochemistry of tears. Surv. Ophthalmol. 26, 84 (1981).
10
Thompson R. N., Napier A., Wekesa K. S., Chemosensory cues from the lacrimal and preputial glands stimulate production of IP3 in the vomeronasal organ and aggression in male mice. Physiol. Behav. 90, 797 (2007).
11
Kimoto H., et al., Sex- and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr. Biol. 17, 1879 (2007).
12
Kimoto H., Haga S., Sato K., Touhara K., Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437, 898 (2005).
13
Frey W. H., DeSota-Johnson D., Hoffman C., McCall J. T., Effect of stimulus on the chemical composition of human tears. Am. J. Ophthalmol. 92, 559 (1981).
14
Gross J. J., Frederickson B. L., Levenson R. W., The psychophysiology of crying. Psychophysiology 31, 460 (1994).
15
This cross-gender method was used because it has been shown to increase the influence of sniffing putative human pheromones (32).
16
Mehrabian A., Epstein N., A measure of emotional empathy. J. Pers. 40, 525 (1972).
17
Bensafi M., et al., Sex-steroid derived compounds induce sex-specific effects on autonomic nervous system function in humans. Behav. Neurosci. 117, 1125 (2003).
18
Levenson R. W., Ekman P., Friesen W. V., Voluntary facial action generates emotion-specific autonomic nervous system activity. Psychophysiology 27, 363 (1990).
19
We refer to this effect on self-rated sexual arousal with caution and describe it as modest because this was the only measure in this manuscript where, by chance, baseline values for saline were lower than for tears, thus generating a potential floor-effect for saline that favored the effect.
20
Wyart C., et al., Smelling a single component of male sweat alters levels of cortisol in women. J. Neurosci. 27, 1261 (2007).
21
Stoléru S. G., Ennaji A., Cournot A., Spira A., LH pulsatile secretion and testosterone blood levels are influenced by sexual arousal in human males. Psychoneuroendocrinology 18, 205 (1993).
22
Sobel N., et al., Blind smell: Brain activation induced by an undetected air-borne chemical. Brain 122, 209 (1999).
23
Lundström 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 (2008).
24
Savic I., Berglund H., Gulyas B., Roland P., Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron 31, 661 (2001).
25
Zhou W., Chen D., Encoding human sexual chemosensory cues in the orbitofrontal and fusiform cortices. J. Neurosci. 28, 14416 (2008).
26
Stern K., McClintock M. K., Regulation of ovulation by human pheromones. Nature 392, 177 (1998).
27
Preti G., Wysocki C. J., Barnhart K. T., Sondheimer S. J., Leyden J. J., Male axillary extracts contain pheromones that affect pulsatile secretion of luteinizing hormone and mood in women recipients. Biol. Reprod. 68, 2107 (2003).
28
Luo M., Fee M. S., Katz L. C., Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299, 1196 (2003).
29
J. M. Masson, S. McCarthy, When Elephants Weep: The Emotional Lives of Animals (Bantam Doubleday Dell, New York, 1995).
30
Wysocki C. J., Preti G., Facts, fallacies, fears, and frustrations with human pheromones. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 281A, 1201 (2004).
31
Jacob S., McClintock M. K., Psychological state and mood effects of steroidal chemosignals in women and men. Horm. Behav. 37, 57 (2000).
32
Jacob S., Hayreh D. J., McClintock M. K., Context-dependent effects of steroid chemosignals on human physiology and mood. Physiol. Behav. 74, 15 (2001).
Information & Authors
Information
Published In
Science
Volume 331 • Issue 6014 • 14 January 2011
Pages: 226 - 230
History
Received: 27 September 2010
Accepted: 17 December 2010
6 January 2011
Copyright
Copyright © 2011, American Association for the Advancement of Science.
