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eLife Volume 10 ,2021-01-04
Oxytocin modulates human chemosensory decoding of sex in a dose-dependent manner
Neuroscience
Kepu Chen 1 Yuting Ye 2 Nikolaus F Troje 3 Wen Zhou 1 , 2 , 4
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DOI:10.7554/eLife.59376
Received 2020-05-27, accepted for publication 2021-01-04, Published 2021-01-04
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摘要

There has been accumulating evidence of human social chemo-signaling, but the underlying mechanisms remain poorly understood. Considering the evolutionarily conserved roles of oxytocin and vasopressin in reproductive and social behaviors, we examined whether the two neuropeptides are involved in the subconscious processing of androsta-4,16,-dien-3-one and estra-1,3,5 (10),16-tetraen-3-ol, two human chemosignals that convey masculinity and femininity to the targeted recipients, respectively. Psychophysical data collected from 216 heterosexual and homosexual men across five experiments totaling 1056 testing sessions consistently showed that such chemosensory communications of masculinity and femininity were blocked by a competitive antagonist of both oxytocin and vasopressin receptors called atosiban, administered nasally. On the other hand, intranasal oxytocin, but not vasopressin, modulated the decoding of androstadienone and estratetraenol in manners that were dose-dependent, nonmonotonic, and contingent upon the recipients’ social proficiency. Taken together, these findings establish a causal link between neuroendocrine factors and subconscious chemosensory communications of sex-specific information in humans.

关键词

Human;biological motion;vasopressin;oxytocin;sex;chemosensory communication

授权许可

© 2021, Chen et al
http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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Kepu Chen,Yuting Ye,Nikolaus F Troje,Wen Zhou. Oxytocin modulates human chemosensory decoding of sex in a dose-dependent manner. eLife ,Vol.10(2021)

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参考文献
[1] TD Wyatt. (2015). The search for human pheromones: the lost decades and the necessity of returning to first principles. Proceedings of the Royal Society B: Biological Sciences.282. DOI: 10.1146/annurev.es.05.110174.001545.
[2] NF Troje. (2002). Decomposing biological motion: a framework for analysis and synthesis of human gait patterns. Journal of Vision.2:2-387. DOI: 10.1146/annurev.es.05.110174.001545.
[3] DB Gower, KT Holland, AI Mallet, PJ Rennie. et al.(1994). 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?. The Journal of Steroid Biochemistry and Molecular Biology.48:409-418. DOI: 10.1146/annurev.es.05.110174.001545.
[4] JN Lundström, T Hummel, MJ Olsson. (2003b). Individual differences in sensitivity to the odor of 4,16-androstadien-3-one. Chemical Senses.28:643-650. DOI: 10.1146/annurev.es.05.110174.001545.
[5] TR Insel, L Young, DM Witt, D Crews. et al.(1993). Gonadal steroids have paradoxical effects on brain oxytocin receptors. Journal of Neuroendocrinology.5:619-628. DOI: 10.1146/annurev.es.05.110174.001545.
[6] B Thysen, WH Elliott, PA Katzman. (1968). Identification of estra-1,3,5(10),16-tetraen-3-ol (estratetraenol) from the urine of pregnant women (1). Steroids.11:73-87. DOI: 10.1146/annurev.es.05.110174.001545.
[7] DB Gower, BA Ruparelia. (1993). Olfaction in humans with special reference to odorous 16-androstenes: their occurrence, perception and possible social, psychological and sexual impact. Journal of Endocrinology.137:167-187. DOI: 10.1146/annurev.es.05.110174.001545.
[8] M Bensafi, WM Brown, R Khan, B Levenson. et al.(2004). Sniffing human sex-steroid derived compounds modulates mood, memory and autonomic nervous system function in specific behavioral contexts. Behavioural Brain Research.152:11-22. DOI: 10.1146/annurev.es.05.110174.001545.
[9] M Manning, A Misicka, A Olma, K Bankowski. et al.(2012). Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. Journal of Neuroendocrinology.24:609-628. DOI: 10.1146/annurev.es.05.110174.001545.
[10] A Benelli, A Bertolini, R Poggioli, B Menozzi. et al.(1995). Polymodal dose-response curve for oxytocin in the social recognition test. Neuropeptides.28:251-255. DOI: 10.1146/annurev.es.05.110174.001545.
[11] C McCall, T Singer. (2012). The animal and human neuroendocrinology of social cognition, motivation and behavior. Nature Neuroscience.15:681-688. DOI: 10.1146/annurev.es.05.110174.001545.
[12] A Gorbman. (1995). Olfactory origins and evolution of the brain-pituitary endocrine system: facts and speculation. General and Comparative Endocrinology.97:171-178. DOI: 10.1146/annurev.es.05.110174.001545.
[13] JA Bartz, JP Nitschke, SA Krol, P-P Tellier. et al.(2019). Oxytocin selectively improves empathic accuracy: a replication in men and novel insights in women. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging.4:1042-1048. DOI: 10.1146/annurev.es.05.110174.001545.
[14] W Zhou, D Chen. (2009). Fear-related chemosignals modulate recognition of fear in ambiguous facial expressions. Psychological Science.20:177-183. DOI: 10.1146/annurev.es.05.110174.001545.
[15] MK McClintock. (1971). Menstrual synchorony and suppression. Nature.229:244-245. DOI: 10.1146/annurev.es.05.110174.001545.
[16] RE Jones, KH Lopez. (2013). Human Reproductive Biology. DOI: 10.1146/annurev.es.05.110174.001545.
[17] P Karlson, M Luscher. (1959). Pheromones': a new term for a class of biologically active substances. Nature.183:55-56. DOI: 10.1146/annurev.es.05.110174.001545.
[18] JA Bartz, J Zaki, N Bolger, KN Ochsner. et al.(2011). Social effects of oxytocin in humans: context and person matter. Trends in Cognitive Sciences.15:301-309. DOI: 10.1146/annurev.es.05.110174.001545.
[19] W Zhou, X Yang, K Chen, P Cai. et al.(2014). Chemosensory communication of gender through two human steroids in a sexually dimorphic manner. Current Biology.24:1091-1095. DOI: 10.1146/annurev.es.05.110174.001545.
[20] DM McNair, M Lorr, LF Droppleman. (1971). Profile of Mood States. DOI: 10.1146/annurev.es.05.110174.001545.
[21] S Baron-Cohen, S Wheelwright, R Skinner, J Martin. et al.(2001). The autism-spectrum quotient (AQ): evidence from asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders.31:5-17. DOI: 10.1146/annurev.es.05.110174.001545.
[22] JA Bartz, J Zaki, N Bolger, E Hollander. et al.(2010). Oxytocin selectively improves empathic accuracy. Psychological Science.21:1426-1428. DOI: 10.1146/annurev.es.05.110174.001545.
[23] Y Ye, Y Zhuang, MAM Smeets, W Zhou. et al.(2019). Human chemosignals modulate emotional perception of biological motion in a sex-specific manner. Psychoneuroendocrinology.100:246-253. DOI: 10.1146/annurev.es.05.110174.001545.
[24] RA Mugford, NW Nowell. (1971). Endocrine control over production and activity of the anti-aggression pheromone from female mice. Journal of Endocrinology.49:225-232. DOI: 10.1146/annurev.es.05.110174.001545.
[25] A Argiolas, GL Gessa. (1991). Central functions of oxytocin. Neuroscience & Biobehavioral Reviews.15:217-231. DOI: 10.1146/annurev.es.05.110174.001545.
[26] S Jacob, MK McClintock. (2000). Psychological state and mood effects of steroidal chemosignals in women and men. Hormones and Behavior.37:57-78. DOI: 10.1146/annurev.es.05.110174.001545.
[27] JH de Groot, MA Smeets, MJ Rowson, PJ Bulsing. et al.(2015). A sniff of happiness. Psychological Science.26:684-700. DOI: 10.1146/annurev.es.05.110174.001545.
[28] RB Simerly. (2002). Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annual Review of Neuroscience.25:507-536. DOI: 10.1146/annurev.es.05.110174.001545.
[29] AC Davison, DV Hinkley. (1997). Bootstrap Methods and Their Application. DOI: 10.1146/annurev.es.05.110174.001545.
[30] I Savic, H Berglund, P Lindström. (2005). Brain response to putative pheromones in homosexual men. PNAS.102:7356-7361. DOI: 10.1146/annurev.es.05.110174.001545.
[31] KJ Parker, JP Garner, RA Libove, SA Hyde. et al.(2014). Plasma oxytocin concentrations and OXTR polymorphisms predict social impairments in children with and without autism spectrum disorder. PNAS.111:12258-12263. DOI: 10.1146/annurev.es.05.110174.001545.
[32] RD Alexander. (1974). The evolution of social behavior. Annual Review of Ecology and Systematics.5:325-383. DOI: 10.1146/annurev.es.05.110174.001545.
[33] LL Oettl, N Ravi, M Schneider, MF Scheller. et al.(2016). Oxytocin enhances social recognition by modulating cortical control of early olfactory processing. Neuron.90:609-621. DOI: 10.1146/annurev.es.05.110174.001545.
[34] K Lancaster, CS Carter, H Pournajafi-Nazarloo, T Karaoli. et al.(2015). Plasma oxytocin explains individual differences in neural substrates of social perception. Frontiers in Human Neuroscience.9. DOI: 10.1146/annurev.es.05.110174.001545.
[35] D Scheele, J Plota, B Stoffel-Wagner, W Maier. et al.(2016). Hormonal contraceptives suppress oxytocin-induced brain reward responses to the partner's face. Social Cognitive and Affective Neuroscience.11:767-774. DOI: 10.1146/annurev.es.05.110174.001545.
[36] NS Koven, LK Max. (2014). Basal salivary oxytocin level predicts extra- but not intra-personal dimensions of emotional intelligence. Psychoneuroendocrinology.44:20-29. DOI: 10.1146/annurev.es.05.110174.001545.
[37] ZR Donaldson, LJ Young. (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. Science.322:900-904. DOI: 10.1146/annurev.es.05.110174.001545.
[38] MJ Olsson, JN Lundström, S Diamantopoulou, F Esteves. et al.(2006). A putative female pheromone affects mood in men differently depending on social context. European Review of Applied Psychology.56:279-284. DOI: 10.1146/annurev.es.05.110174.001545.
[39] M Kosfeld, M Heinrichs, PJ Zak, U Fischbacher. et al.(2005). Oxytocin increases trust in humans. Nature.435:673-676. DOI: 10.1146/annurev.es.05.110174.001545.
[40] C Cardoso, MA Ellenbogen, MA Orlando, SL Bacon. et al.(2013). Intranasal oxytocin attenuates the cortisol response to physical stress: a dose-response study. Psychoneuroendocrinology.38:399-407. DOI: 10.1146/annurev.es.05.110174.001545.
[41] KJ Parker, O Oztan, RA Libove, RD Sumiyoshi. et al.(2017). Intranasal oxytocin treatment for social deficits and biomarkers of response in children with autism. PNAS.114:8119-8124. DOI: 10.1146/annurev.es.05.110174.001545.
[42] CS Carter. (1992). Oxytocin and sexual behavior. Neuroscience & Biobehavioral Reviews.16:131-144. DOI: 10.1146/annurev.es.05.110174.001545.
[43] M Cusson, JN McNeil. (1989). Involvement of juvenile hormone in the regulation of pheromone release activities in a moth. Science.243:210-212. DOI: 10.1146/annurev.es.05.110174.001545.
[44] CS Carter. (2014). Oxytocin pathways and the evolution of human behavior. Annual Review of Psychology.65:17-39. DOI: 10.1146/annurev.es.05.110174.001545.
[45] JD Tang, RE Charlton, RA Jurenka, WA Wolf. et al.(1989). Regulation of pheromone biosynthesis by a brain hormone in two moth species. PNAS.86:1806-1810. DOI: 10.1146/annurev.es.05.110174.001545.
[46] AS Ghuman, JR McDaniel, A Martin. (2010). Face adaptation without a face. Current Biology.20:32-36. DOI: 10.1146/annurev.es.05.110174.001545.
[47] Y Endevelt-Shapira, O Perl, A Ravia, D Amir. et al.(2018). Altered responses to social chemosignals in autism spectrum disorder. Nature Neuroscience.21:111-119. DOI: 10.1146/annurev.es.05.110174.001545.
[48] SM Freeman, S Samineni, PC Allen, D Stockinger. et al.(2016). Plasma and CSF oxytocin levels after intranasal and intravenous oxytocin in awake macaques. Psychoneuroendocrinology.66:185-194. DOI: 10.1146/annurev.es.05.110174.001545.
[49] JN Lundström, M Gonçalves, F Esteves, MJ Olsson. et al.(2003a). Psychological effects of subthreshold exposure to the putative human pheromone 4,16-androstadien-3-one. Hormones and Behavior.44:395-401. DOI: 10.1146/annurev.es.05.110174.001545.
[50] FB Spengler, J Schultz, D Scheele, M Essel. et al.(2017). Kinetics and dose dependency of intranasal oxytocin effects on amygdala reactivity. Biological Psychiatry.82:885-894. DOI: 10.1146/annurev.es.05.110174.001545.
[51] I Savic, H Berglund, B Gulyas, P Roland. et al.(2001). Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron.31:661-668. DOI: 10.1146/annurev.es.05.110174.001545.
[52] K Stern, MK McClintock. (1998). Regulation of ovulation by human pheromones. Nature.392:177-179. DOI: 10.1146/annurev.es.05.110174.001545.
[53] AK Raina, H Jaffe, TG Kempe, P Keim. et al.(1989). Identification of a neuropeptide hormone that regulates sex pheromone production in female moths. Science.244:796-798. DOI: 10.1146/annurev.es.05.110174.001545.
[54] S Lundin, M Akerlund, PO Fagerström, A Hauksson. et al.(1986). Pharmacokinetics in the human of a new synthetic vasopressin and oxytocin uterine antagonist. Acta Endocrinologica.112:465-472. DOI: 10.1146/annurev.es.05.110174.001545.
[55] R Stoop. (2012). Neuromodulation by oxytocin and vasopressin. Neuron.76:142-159. DOI: 10.1146/annurev.es.05.110174.001545.
[56] DS Quintana, LT Westlye, S Hope, T Nærland. et al.(2017). Dose-dependent social-cognitive effects of intranasal oxytocin delivered with novel breath powered device in adults with autism spectrum disorder: a randomized placebo-controlled double-blind crossover trial. Translational Psychiatry.7. DOI: 10.1146/annurev.es.05.110174.001545.
[57] R Liu, X Yuan, K Chen, Y Jiang. et al.(2018). Perception of social interaction compresses subjective duration in an oxytocin-dependent manner. eLife.7. DOI: 10.1146/annurev.es.05.110174.001545.
[58] HH Lin, DS Cao, S Sethi, Z Zeng. et al.(2016). Hormonal modulation of pheromone detection enhances male courtship success. Neuron.90:1272-1285. DOI: 10.1146/annurev.es.05.110174.001545.
[59] H Berglund, P Lindström, I Savic. (2006). Brain response to putative pheromones in lesbian women. PNAS.103:8269-8274. DOI: 10.1146/annurev.es.05.110174.001545.
[60] AM Blouin, I Fried, CL Wilson, RJ Staba. et al.(2013). Human hypocretin and melanin-concentrating hormone levels are linked to emotion and social interaction. Nature Communications.4. DOI: 10.1146/annurev.es.05.110174.001545.
[61] J Born, T Lange, W Kern, GP McGregor. et al.(2002). Sniffing neuropeptides: a transnasal approach to the human brain. Nature Neuroscience.5:514-516. DOI: 10.1146/annurev.es.05.110174.001545.