Social laughter triggers endogenous opioid release in humans

Journal of Neuroscience

Volumn 37, Issue 25, 2017, Pages 6125-6131

  Manninen, Sandra ^a   Tuominen, Lauri ^a   Dunbar, Robin I ^b,c   Karjalainen, Tomi ^a   Hirvonen, Jussi ^a   Arponen, Eveliina ^a   Hari, Riitta ^b   Jääskeläinen, Iiro P ^b   Sams, Mikko ^b   Nummenmaa, Lauri ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b AALTO UNIVERSITY   (Finland)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Bonding; Carfentanil; Emotion; Laughter; Opioids; Positron emission tomography

Indexed keywords

ENDORPHIN; MU OPIATE RECEPTOR; OPRM1 PROTEIN, HUMAN;

ADULT; ARTICLE; CONTROLLED STUDY; FEMALE; HAPPINESS; HUMAN; HUMAN EXPERIMENT; IRRITABILITY; LAUGHTER; LITERATURE; MALE; NEUROCHEMISTRY; NEUROPHYSIOLOGY; PAIN; PAIN THRESHOLD; PLEASURE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SOCIAL BEHAVIOR; SOCIAL BONDING; SOMNOLENCE; TENSION; VISUAL ANALOG SCALE; BRAIN CHEMISTRY; BRAIN MAPPING; DRUG EFFECTS; METABOLISM; OBJECT RELATION; PHYSIOLOGY; SOCIAL ENVIRONMENT; YOUNG ADULT;

ADULT; BRAIN CHEMISTRY; BRAIN MAPPING; ENDORPHINS; FEMALE; HUMANS; LAUGHTER; MALE; OBJECT ATTACHMENT; PLEASURE; POSITRON-EMISSION TOMOGRAPHY; RECEPTORS, OPIOID, MU; SOCIAL ENVIRONMENT; YOUNG ADULT;

EID: 85021120072     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0688-16.2017     Document Type: Article

References (55)

1. Alenius S, Ruotsalainen U (1997) Bayesian image reconstruction for emission tomography based on median root prior. Eur J Nucl Med 24:258-265. CrossRef
2. Barr CS, Schwandt ML, Lindell SG, Higley JD, Maestripieri D, Goldman D, Suomi SJ, Heilig M (2008) Variation at the mu-opioid receptor gene (OPRM1) influences attachment behavior in infant primates. Proc Natl Acad Sci U S A 105:5277–5281. CrossRef Medline
3. Berk LS, Tan SA, Fry WF, Napier BJ, Lee JW, Hubbard RW, Lewis JE, Eby WC (1989) Neuroendocrine and stress hormone changes during mirthful laughter. Am J Med Sci 298:390-396. CrossRef Medline
4. Broadhead WE, Kaplan BH, James SA, Wagner EH, Schoenbach VJ, Grimson R, Heyden S, Tibblin G, Gehlbach SH (1983) The epidemiologic evidence for a relationship between social support and health. Am J Epidemiol 117:521–537. CrossRef Medline
5. Colasanti A, Rabiner EA, Lingford-Hughes A, Nutt DJ (2011) Opioids and anxiety. J Psychopharmacol 25:1415–1433. CrossRef Medline
6. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189-195. CrossRef Medline
7. Curry OS, Dunbar RIM (2013) Sharing a joke: the effects of a similar sense of humor on affiliation and altruism. Evolution and Human Behavior 34:125–129. CrossRef
8. Darwin C (1872) Expression of the emotions in man and animals. London: John Murray.
9. Davila Ross M, Owren MJ, Zimmermann E (2009) Reconstructing the evolution of laughter in great apes and humans. Curr Biol 19:1106-1111. CrossRef Medline
10. Dunbar RI (1991) Functional significance of social grooming in primates. Folia Primatologica 57:121–131. CrossRef
11. Dunbar RI (2008) Mind the gap: or why humans aren’t just great apes. Proceedings of the British Academy 154:403-423.
12. Dunbar RI (2012) Bridging the bonding gap: the transition from primates to humans. Philos Trans R Soc Lond B Biol Sci 367:1837–1846. CrossRef Medline
13. Dunbar RI, Shultz S (2010) Bondedness and sociality. Behaviour 147:775-803.
14. Dunbar RI, Baron R, Frangou A, Pearce E, van Leeuwen EJ, Stow J, Partridge G, MacDonald I, Barra V, van Vugt M (2012) Social laughter is correlated with an elevated pain threshold. Proc Biol Sci 279:1161–1167. CrossRef Medline
15. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitec-tonic maps and functional imaging data. Neuroimage 25:1325–1335. CrossRef Medline
16. Fabre-Nys C, Meller RE, Keverne EB (1982) Opiate antagonists stimulate affiliative behaviour in monkeys. Pharmacol Biochem Behav 16:653-659. CrossRef Medline
17. Gabilondo AM, Meana JJ, García-Sevilla JA (1995) Increased density of mu-opioid receptors in the postmortem brain of suicide victims. Brain Res 682:245–250. CrossRef Medline
18. Graves FC, Wallen K, Maestripieri D (2002) Opioids and attachment in rhesus macaque (Macaca mulatta) abusive mothers. Behav Neurosci 116: 489-493. CrossRef Medline
19. Gunn RN, Lammertsma AA, Hume SP, Cunningham VJ (1997) Parametric imaging of ligand-receptor binding in PET using a simplified reference region model. Neuroimage 6:279-287. CrossRef Medline
20. Henriksen G, Willoch F (2008) Imaging of opioid receptors in the central nervous system. Brain 131:1171–1196. CrossRef Medline
21. Hiller JM, Fan LQ (1996) Laminar distribution of the multiple opioid receptors in the human cerebral cortex. Neurochem Res 21:1333–1345. CrossRef Medline
22. Hirvonen J, Aalto S, Hagelberg N, Maksimow A, Ingman K, Oikonen V, Virkkala J, Någren K, Scheinin H (2009) Measurement of central mu-opioid receptor binding in vivo with PET and [11C]carfentanil: a test-retest study in healthy subjects. Eur J Nucl Med Mol Imaging 36:275–286. CrossRef Medline
23. Holt-Lunstad J, Smith TB, Baker M, Harris T, Stephenson D (2015) Loneliness and social isolation as risk factors for mortality: a meta-analytic review. Perspect Psychol Sci 10:227–237. CrossRef Medline
24. Hsu DT, Sanford BJ, Meyers KK, Love TM, Hazlett KE, Wang H, Ni L, Walker SJ, Mickey BJ, Korycinski ST, Koeppe RA, Crocker JK, Langenecker SA, Zubieta JK (2013) Response of the μ-opioid system to social rejection and acceptance. Mol Psychiatry 18:1211–1217. CrossRef Medline
25. Karlsson HK, Tuominen L, Tuulari JJ, Hirvonen J, Parkkola R, Helin S, Salmi-nen P, Nuutila P, Nummenmaa L (2015) Obesity is associated with decreased mu-opioid but unaltered dopamine D-2 receptor availability in the brain. J Neurosci 35:3959-3965. CrossRef Medline
26. Kätsyri J, Hari R, Ravaja N, Nummenmaa L (2013) The opponent matters: elevated fMRI reward responses to winning against a human versus a computer opponent during interactive video game playing. Cereb Cortex 23:2829-2839. CrossRef Medline
27. Kennedy SE, Koeppe RA, Young EA, Zubieta JK (2006) Dysregulation of endogenous opioid emotion regulation circuitry in major depression in women. Arch Gen Psychiatry 63:1199-1208. CrossRef Medline
28. Keverne EB, Martensz ND, Tuite B (1989) Beta-endorphin concentrations in cerebrospinal-fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology 14:155–161. CrossRef Medline
29. Liu L, Newschaffer CJ (2011) Impact of social connections on risk of heart disease, cancer, and all-cause mortality among elderly Americans: Findings from the Second Longitudinal Study of Aging (LSOA II). Arch Gerontol Geriatr 53:168-173. CrossRef Medline
30. Meller RE, Keverne EB, Herbert J (1980) Behavioral and endocrine effects of naltrexone in male talapoin monkeys. Pharmacol Biochem Behav 13:663-672. CrossRef Medline
31. Mireault GC, Crockenberg SC, Sparrow JE, Cousineau K, Pettinato C, Woodard K (2015) Laughing matters: Infant humor in the context of parental affect. J Exp Child Psychol 136:30-41. CrossRef Medline
32. Moles A, Kieffer BL, D’Amato FR (2004) Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science 304:1983–1986. CrossRef Medline
33. Nummenmaa L, Tuominen LJ (2017) Opioid system and human emotions. Br J Pharmacol. In press.
34. Nummenmaa L, Manninen S, Tuominen L, Hirvonen J, Kalliokoski KK, Nuutila P, Jääskeläinen IP, Hari R, Dunbar RI, Sams M (2015) Adult attachment style Is associated with cerebral μ-opioid receptor availability in humans. Hum Brain Mapp 36:3621–3628. CrossRef Medline
35. Olausson H, Lamarre Y, Backlund H, Morin C, Wallin BG, Starck G, Ekholm S, Strigo I, Worsley K, Vallbo AB, Bushnell MC (2002) Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 5:900-904. CrossRef Medline
36. Panksepp J, Herman BH, Vilberg T, Bishop P, DeEskinazi FG (1980) Endogenous opioids and social behaviour. Neurosci Biobehav Rev 4:473–487. CrossRef Medline
37. Peciña M, Zubieta JK (2015) Molecular mechanisms of placebo responses in humans. Mol Psychiatry 20:416-423. CrossRef Medline
38. Preuschoft S (1992) “Laughter” and “smile” in Barbary macaques (Macaca sylvanus). Ethology 91:220-236.
39. Provine RR (2004) Laughing, tickling, and the evolution of speech and self. Curr Dir Psychol Sci 13:215–218. CrossRef
40. Rütgen M, Seidel EM, Riečanský I, Lamm C (2015a) Reduction of empathy for pain by placebo analgesia suggests functional equivalence of empathy and first-hand emotion experience. J Neurosci 35:8938-8947. CrossRef Medline
41. Rütgen M, Seidel EM, Silani G, Riečanský I, Hummer A, Windischberger C, Petrovic P, Lamm C (2015b) Placebo analgesia and its opioidergic regulation suggest that empathy for pain is grounded in self pain. Proc Natl Acad Sci U S A 112:E5638-E5646. CrossRef Medline
42. Sander CY, Hooker JM, Wey HY, Wilson CM, Catana C, Rosen B, Mandeville JB (2014) Effects of simultaneously measured flow changes on D2/D3 radiotracer dynamics. In: 10th International symposium on functional neuroreceptor mapping of the living brain. Amsterdam.
43. Sander K, Scheich H (2005) Left auditory cortex and amygdala, but right insula dominance for human laughing and crying. J Cogn Neurosci 17: 1519-1531. CrossRef Medline
44. Sauter DA, Eisner F, Ekman P, Scott SK (2010) Cross-cultural recognition of basic emotions through nonverbal emotional vocalizations. Proc Natl Acad Sci U S A 107:2408-2412. CrossRef Medline
45. Scott SK, Lavan N, Chen S, McGettigan C (2014) The social life of laughter. Trends Cogn Sci 18:618-620. CrossRef Medline
46. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234. CrossRef Medline
47. Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303:1157–1162. CrossRef Medline
48. Suvilehto JT, Glerean E, Dunbar RI, Hari R, Nummenmaa L (2015) Topography of social touching depends on emotional bonds between humans. Proc Natl Acad Sci U S A 112:13811–13816. CrossRef Medline
49. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289. CrossRef Medline
50. Waller B, Dunbar R (2005) Differential behavioural effects of silent bared teeth display and relaxed open mouth display in chimpanzees (Pan trog-lodytes). Ethology 111:129-142. CrossRef
51. Way BM, Taylor SE, Eisenberger NI (2009) Variation in the mu-opioid receptor gene (OPRM1) is associated with dispositional and neural sensitivity to social rejection. Proc Natl Acad Sci U S A 106:15079-15084. CrossRef Medline
52. Wicker B, Keysers C, Plailly J, Royet JP, Gallese V, Rizzolatti G (2003) Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Neuron 40:655-664. CrossRef Medline
53. Wild B, Rodden FA, Grodd W, Ruch W (2003) Neural correlates of laughter and humour. Brain 126:2121–2138. CrossRef Medline
54. Young LJ, Lim MM, Gingrich B, Insel TR (2001) Cellular mechanisms of social attachment. Horm Behav 40:133–138. CrossRef Medline
55. Zubieta JK, Dannals RF, Frost JJ (1999) Gender and age influences on human brain mu-opioid receptor binding measured by PET. Am J Psychiatry 156:842-848. CrossRef Medline