Opiate antagonists stimulate affiliative behaviour in monkeys
Abstract
The effects of treating captive talapoin monkeys acutely (twice daily for 7 days) with naltrexone hydrochloride (0.25 mg 0.5 mg and 1 mg/kg intramuscular injections twice daily), naloxone hydrochloride (0.5 mg/kg IM twice daily) and sulpiride (1.5 mg/kg IM twice daily) was studied in social pairs and singly caged animals. The behaviour of social pairs and endocrine changes in all treated monkeys were monitored before, during and after withdrawal of the course of drug treatment. Naltrexone and naloxone, but not sulpiride, significant increased grooming and grooming invitations while aggressive behaviour, self grooming, scratching and general locomotor activity were unaffected. There was an overall increase in LH, testosterone and cortisol in plasma samples taken 60 mins after opiate receptor blockade. Prolactin was unchanged but increased dramatically in animals treated with sulpiride. No significant endocrine changes were observed to precede the increased grooming behaviour which opiate receptor blockade induced. The behavioural changes reported for this primate support the view that positive affect arising from social bonds may be mediated by cerebral endorphin containing systems.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Opioid agonists, such as morphine, decrease physical contact between social partners, whereas naloxone administration increases solicitation for social contact, such as grooming and proximity.
“opioid agonists, such as morphine, decrease physical contact between social partners, whereas NAL administration increases solicitation for social contact, such as grooming and proximity (16–19).”
From Oxytocin under opioid antagonism leads to supralinear enhancement of social attention (2017) · cites this paper as [17]
The μ-opioid receptor is the target of β-endorphin, which seems to play an important role in maintaining social bonds in primates (including humans).
“The μ -opioid receptor (16) has been of particular interest because it is the target of β -endorphin, which seems to play an important role in maintaining social bonds in primates (including humans) (17 -19).”
From Variation in the β-endorphin, oxytocin, and dopamine receptor genes is associated with different dimensions of human sociality (2017) · cites this paper as [17]
Cites
β-Endorphin and Adrenocorticotropin Are Selected Concomitantly by the Pituitary Gland
Guillemin, R., Vargo, T., Rossier, J., Minick, S., Ling, N., Rivier, C., Vale, W., & Bloom, F. (1977) · Science · doi:10.1126/science.197601 · Cited by 1,419 · see citing works
Advances in biochemical psychopharmacology
Aprison, M. H. (1970) · Neuropharmacology · doi:10.1016/0028-3908(70)90062-6 · Cited by 1,177 · see citing works
Endorphins: Profound Behavioral Effects in Rats Suggest New Etiological Factors in Mental Illness
Bloom, F. E., Segal, D., LING, N. C., & Guillemin, R. (1976) · Science · doi:10.1126/science.185694 · Cited by 810 · see citing works
Stress-induced parallel changes in central opioid levels and pain responsiveness in the rat
Madden, J. J., Akil, H., Patrick, R. L., & Barchas, J. D. (1977) · Nature · doi:10.1038/265358a0 · Cited by 559 · see citing works
Biological bases of human social behaviour
Hinde, R. A. (1974) · Andalas University Repository (Andalas University) · Cited by 505 · see citing works
The biology of social attachments: opiates alleviate separation distress.
Panksepp, J., Herman, B., Conner, R., Bishop, P., & Scott, J. P. (1978) · PubMed · Cited by 473 · see citing works
Clement-Jones, V., Tomlin, S., Rees, L., Mcloughlin, L., Besser, G., & Wen, H.-L. (1980) · The Lancet · doi:10.1016/s0140-6736(80)92106-6 · Cited by 398 · see citing works
The role of endorphins in stress: Evidence and speculations
Amir, S., Brown, Z. W., & Amit, Z. (1980) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(80)90027-5 · Cited by 351 · see citing works
Herman, B. H., & Panksepp, J. (1978) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(78)90167-3 · Cited by 330 · see citing works
Cicero, T., Schainker, B., & Meyer, E. (1979) · Endocrinology · doi:10.1210/endo-104-5-1286 · Cited by 328 · see citing works
Suppression of deprivation-induced food and water intake in rats and mice by naloxone.
Brown, D. R., & Holtzman, S. (1979) · Pharmacology, Biochemistry and Behavior · doi:10.1016/0091-3057(79)90043-1 · Cited by 271 · see citing works
Naloxone-induced reversal of schizophrenic hallucinations
Gunne, L. M., Lindstr�m, L. H., & Terenius, L. Y. (1977) · Journal of Neural Transmission · doi:10.1007/bf01250276 · Cited by 263 · see citing works
β-ENDORPHIN AND ADRENOCORTICOTROPIN ARE SECRETED CONCOMITANTLY BY THE PITUITARY GLAND
Guillemin, R., Vargo, T. M., Rossier, J., Minick, S., LING, N. C., RIVIER, C. L., Vale, W., & Bloom, F. E. (1978) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-197803000-00017 · Cited by 243 · see citing works
Induction of Copulatory Behavior in Sexually Inactive Rats by Naloxone
Gessa, G. L., Paglietti, E., & Quarantotti, B. P. (1979) · Science · doi:10.1126/science.432642 · Cited by 215 · see citing works
Opioid Peptides Modulate Luteinizing Hormone Secretion During Sexual Maturation
Blank, M. S., Panerai, A. E., & Friesen, H. G. (1979) · Science · doi:10.1126/science.424743 · Cited by 199 · see citing works
Naloxone increases ACTH and cortisol levels in man.
Volavka, J., Cho, D., Mallya, A., & Bauman, J. (1979) · New England Journal of Medicine · doi:10.1056/nejm197905033001817 · Cited by 196 · see citing works
β-Endorphin and male sexual behavior
Meyerson, B. J., & Terenius, L. Y. (1977) · European Journal of Pharmacology · doi:10.1016/0014-2999(77)90359-4 · Cited by 171 · see citing works
Effects of naloxone on experimentally induced ischemic pain and on mood in human subjects.
Grevert, P., & Goldstein, A. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.3.1291 · Cited by 153 · see citing works
INHIBITION OF THE RELEASE OF PITUITARY OVULATORY HORMONE IN THE RAT BY MORPHINE1
Barraclough, C. A., & Sawyer, C. H. (1955) · Endocrinology · doi:10.1210/endo-57-3-329 · Cited by 146 · see citing works
Effects of naltrexone on mood and neuroendocrine function in normal adult males
Mendelson, J. H. (1978) · Psychoneuroendocrinology · doi:10.1016/0306-4530(78)90013-6 · Cited by 145 · see citing works
Endogenous opiates block dopamine inhibition of prolactin secretion in vitro
Enjalbert, A., Ruberg, M., Arancibia, S., Priam, M., & Kordon, C. (1979) · Nature · doi:10.1038/280595a0 · Cited by 138 · see citing works
Effects of heroin and methadone on plasma cortisol and testosterone.
Mendelson, J., Meyer, R., Ellingboe, J., Mirin, S., & Mcdougle, M. (1975) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)30341-1 · Cited by 132 · see citing works
Cicero, T. J., Meyer, E. R., Bell, R. D., & KOCH, G. A. (1976) · Endocrinology · doi:10.1210/endo-98-2-367 · Cited by 115 · see citing works
THE EFFECT OF HEROIN ADDICTION ON PITUITARY‐TESTICULAR FUNCTION
Wang, C., Chan, V., & YEUNG, R. T. T. (1978) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1978.tb03585.x · Cited by 109 · see citing works
Behavioural and endocrine effects of naltrexone in male talapoin monkeys.
Meller, R. E., Keverne, E., & Herbert, J. (1980) · Pharmacology, Biochemistry and Behavior · doi:10.1016/0091-3057(80)90010-6 · Cited by 97 · see citing works
The Development of Sociosexual Behaviours in Japanese Macaques Macaca Fuscata
Hanby, J. P., & Brown, C. E. (1974) · Behaviour · doi:10.1163/156853974x00444 · Cited by 84 · see citing works
beta-Endorphin and naloxone in psychiatric patients: clinical and biological effects
Lehmann, H., Nair, N. P., & Kline, N. S. (1979) · American Journal of Psychiatry · doi:10.1176/ajp.136.6.762 · Cited by 72 · see citing works
MICHAEL, R. P., Herbert, J., & WELEGALLA, J. (1966) · Journal of Endocrinology · doi:10.1677/joe.0.0360263 · Cited by 55 · see citing works
Sexual and Aggressive Behaviour in Social Groups of Talapoin Monkeys
Keverne, E. B. (1979) · Novartis Foundation symposium · doi:10.1002/9780470720448.ch13 · Cited by 48 · see citing works
The regional distribution of immunoreactive β-endorphin in the monkey brain
Matsukura, S., Yoshimi, H., Sueoka, S., Kataoka, K., Ono, T., & OHGUSHI, N. (1978) · Brain Research · doi:10.1016/0006-8993(78)90125-7 · Cited by 42 · see citing works
PROLACTIN SECRETION, A MEASURABLE CENTRAL EFFECT OF OPIATE-RECEPTOR ANTAGONISTS
Gold, M. S., Redmond, D. E., & DONABEDIAN, R. K. (1978) · The Lancet · doi:10.1016/s0140-6736(78)90089-2 · Cited by 37 · see citing works
Systemic administration of endorphins selectively alters open field behavior of rats
Veith, J. L., Sandman, C. A., Walker, J. M., Coy, D. H., & Kastin, A. J. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90243-3 · Cited by 35 · see citing works
Rodgers, R. J., & File, S. E. (1979) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(79)90033-9 · Cited by 34 · see citing works
Eysenck, H. J. (1979) · Behaviour Research and Therapy · doi:10.1016/0005-7967(79)90118-9 · Cited by 29 · see citing works
Effects of heroin and naltrexone on plasma prolactin levels in man
Ellingboe, J., Mendelson, J. H., & Kuehnle, J. C. (1980) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(80)90431-1 · Cited by 28 · see citing works
β-endorphin: Pharmacologic and behavioral activity in cats after low intravenous doses
Catlin, D. H., George, R., & Li, C. (1978) · Life Sciences · doi:10.1016/0024-3205(78)90188-1 · Cited by 26 · see citing works
Kapp, B. S., & Gallagher, M. (1979) · Trends in Neurosciences · doi:10.1016/0166-2236(79)90072-9 · Cited by 20 · see citing works
Participation of hypothalamic endorphins in the control of prolactin release.
Guidotti, A., & Grandison, L. (1978) · PubMed · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Baron-Cohen, S., Ring, H. A., Bullmore, E. T., Wheelwright, S., Ashwin, C., & Williams, S. C. R. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00011-7 · Cited by 1,130 · see citing works
Eisenberger, N. I. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3231 · Cited by 1,016 · see citing works
Keverne, E. B., Martensz, N. D., & Tuite, B. (1989) · Psychoneuroendocrinology · doi:10.1016/0306-4530(89)90065-6 · Cited by 525 · see citing works
“This is further supported by the finding that endogenous opiate withdrawal by receptor blockade with naltrexone enhances the need for social attachment (Meller et al., 1980; Fabre-Nys et al., 1982).”
BackgroundThe compulsion to repeat the trauma. Re-enactment, revictimization, and masochism.
van der Kolk, B. A. (1989) · PubMed · Cited by 500 · see citing works
Insel, T. R. (1992) · Psychoneuroendocrinology · doi:10.1016/0306-4530(92)90073-g · Cited by 487 · see citing works
The Compulsion to Repeat the Trauma
van der Kolk, B. A. (1989) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(18)30439-8 · Cited by 629 · see citing works
Topography of social touching depends on emotional bonds between humans
Suvilehto, J. T., Glerean, E., Dunbar, R. I. M., Hari, R., & Nummenmaa, L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1519231112 · Cited by 385 · see citing works
“In primates, opioid-receptor antagonists increase the frequency of grooming (27, 30) and grooming solicitations (31) irrespective of the dyadic relationship (32).”
BackgroundDunbar, R. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.10.004 · Cited by 380 · see citing works
Time to connect: bringing social context into addiction neuroscience
Heilig, M., Epstein, D. H., Nader, M. A., & Shaham, Y. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.67 · Cited by 298 · see citing works
Singing and social bonding: changes in connectivity and pain threshold as a function of group size
Weinstein, D., Launay, J., Pearce, E., Dunbar, R. I. M., & Stewart, L. (2016) · Evolution and Human Behavior · doi:10.1016/j.evolhumbehav.2015.10.002 · Cited by 275 · see citing works
“, 1995), and blocking endorphin receptors leads to increased grooming rates (Fabre-Nys et al., 1982;Meller et al., 1980).”
Opioid therapy for chronic pain in the United States: Promises and perils
Sullivan, M. D., & Howe, C. Q. (2013) · Pain · doi:10.1016/j.pain.2013.09.009 · Cited by 231 · see citing works
“Opioid agonists have been found to reduce efforts at social affiliation in mammals [36], while opioid antagonists increase efforts at social affiliation [23].”
BackgroundSocial Laughter Triggers Endogenous Opioid Release in Humans
Manninen, S., Tuominen, L., Dunbar, R. I., Karjalainen, T., Hirvonen, J., Arponen, E., Hari, R., Jääskeläinen, I. P., Sams, M., & Nummenmaa, L. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.0688-16.2017 · Cited by 213 · see citing works
PANKSEPP, J., NELSON, E., & BEKKEDAL, M. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51914.x · Cited by 210 · see citing works
Opioids for the Treatment of Chronic Pain: Mistakes Made, Lessons Learned, and Future Directions
Ballantyne, J. C. (2017) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000002500 · Cited by 203 · see citing works
Synchrony as an Adaptive Mechanism for Large‐Scale Human Social Bonding
Launay, J., Tarr, B., & Dunbar, R. (2016) · Ethology · doi:10.1111/eth.12528 · Cited by 202 · see citing works
Oxytocin Facilitation of Maternal Behavior in Sheepa
Keverne, E. B., & Kendrick, K. M. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34348.x · Cited by 183 · see citing works
Opioid system and human emotions
Nummenmaa, L., & Tuominen, L. (2018) · British Journal of Pharmacology · doi:10.1111/bph.13812 · Cited by 178 · see citing works
“Opioid antagonists promote social grooming and grooming solicitations in nonhuman primates, suggesting that endogenous opioid tone modulates attachment behaviour (Fabre-Nys et al., 1982; Keverne et al., 1989; Graves et al., 2002).”
BackgroundSocial touch modulates endogenous μ-opioid system activity in humans
Nummenmaa, L., Tuominen, L. J., Dunbar, R., Hirvonen, J., Manninen, S., Arponen, E., Machin, A., Hari, R., Jääskeläinen, I. P., & Sams, M. E. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.05.063 · Cited by 170 · see citing works
van der Kolk, B. A. (1988) · Journal of Traumatic Stress · doi:10.1007/bf00974765 · Cited by 202 · see citing works
The biology of human parenting: insights from nonhuman primates
Dario Maestripieri, A. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00042-6 · Cited by 152 · see citing works
“[16] Fabre-Nys C, Meller RE, Keverne EB.”
BackgroundThe Psychopharmacology of Aggression
Miczek, K. A. (1987) · Springer eBooks · doi:10.1007/978-1-4613-1819-4_4 · Cited by 145 · see citing works
Borderline personality disorder: a dysregulation of the endogenous opioid system?
Bandelow, B., Schmahl, C., Falkai, P., & Wedekind, D. (2010) · Psychological Review · doi:10.1037/a0018095 · Cited by 135 · see citing works
Adult attachment style is associated with cerebral μ‐opioid receptor availability in humans
Nummenmaa, L., Manninen, S., Tuominen, L., Hirvonen, J., Kalliokoski, K. K., Nuutila, P., Jääskeläinen, I. P., Hari, R., Dunbar, R. I. M., & Sams, M. (2015) · Human Brain Mapping · doi:10.1002/hbm.22866 · Cited by 133 · see citing works
Pearce, E., Wlodarski, R., Machin, A., & Dunbar, R. I. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1700712114 · Cited by 131 · see citing works
Relationship assessment through emotional mediation
Aureli, F., & Schaffner, C. M. (2002) · Behaviour · doi:10.1163/156853902760102726 · Cited by 128 · see citing works
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00004-8 · Cited by 128 · see citing works
Opiate systems in mother and infant primates coordinate intimate contact during reunion
Kalin, N. H., Shelton, S. E., & Lynn, D. E. (1995) · Psychoneuroendocrinology · doi:10.1016/0306-4530(95)00023-2 · Cited by 122 · see citing works
“, 1989); and increases grooming in talapoin monkeys (Fabre-Nys et al., 1982; Keveme et al., 1989; Meller et al., 1980).”
BackgroundState-dependent μ-opioid modulation of social motivation
Løseth, G. E., Ellingsen, D., & Leknes, S. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00430 · Cited by 116 · see citing works
“…et al., 1989), while those injected with μ-opioid antagonists such as naltrexone and naloxone made more solicitations and spent more time receiving grooming (Meller et al., 1980; Fabre-Nys et al., 1982; Keverne et al., 1989; Schino and Troisi, 1992; Martel et al., 1995; Graves et al., 2002).”
BackgroundHowe, C., & Sullivan, M. (2014) · General Hospital Psychiatry · doi:10.1016/j.genhosppsych.2013.10.003 · Cited by 107 · see citing works
“Later in life, opioid agonists reduce efforts at social affiliation [102,103] while opioid antagonists increase efforts at social affiliation [104].”
BackgroundSaturable transport of peptides across the blood-brain barrier
Banks, W. A., & Kastin, A. J. (1987) · Life Sciences · doi:10.1016/0024-3205(87)90606-0 · Cited by 114 · see citing works
Martel, F. L., Nevison, C. M., Simpson, M. J. A., & Keverne, E. B. (1995) · Developmental Psychobiology · doi:10.1002/dev.420280202 · Cited by 111 · see citing works
Self-citationThe Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50006-8 · Cited by 109 · see citing works
Neurobiology of Loneliness, Isolation, and Loss: Integrating Human and Animal Perspectives
Vitale, E. M., & Smith, A. S. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.846315 · Cited by 112 · see citing works
Social isolation and the brain in the pandemic era
Bzdok, D., & Dunbar, R. I. M. (2022) · Nature Human Behaviour · doi:10.1038/s41562-022-01453-0 · Cited by 100 · see citing works
Endogenous opioids: Do they modulate the rat pup's response to social isolation?
Winslow, J., & Insel, T. R. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.2.253 · Cited by 85 · see citing works
Oxytocin Receptors and Maternal Behavior
Insel, T. R., & SHAPIRO, L. E. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34350.x · Cited by 79 · see citing works
Laughter and its role in the evolution of human social bonding
Dunbar, R. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0176 · Cited by 79 · see citing works
Emergent Patterns of Social Affiliation in Primates, a Model
Puga‐Gonzalez, I., Hildenbrandt, H., & Hemelrijk, C. K. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000630 · Cited by 78 · see citing works
Central mechanisms underlying the neural and neuroendocrine determinants of maternal behaviour
Keverne, E. B. (1988) · Psychoneuroendocrinology · doi:10.1016/0306-4530(88)90010-8 · Cited by 78 · see citing works
Opioid receptor blockade reduces maternal affect and social grooming in rhesus monkeys
Martel, F. L., Nevison, C. M., Rayment, F. D., Simpson, M. J. A., & Keverne, E. B. (1993) · Psychoneuroendocrinology · doi:10.1016/0306-4530(93)90027-i · Cited by 75 · see citing works
Self-citationSocial Monogamy in Nonhuman Primates: Phylogeny, Phenotype, and Physiology
French, J. A., Cavanaugh, J., Mustoe, A. C., Carp, S. B., & Womack, S. L. (2017) · The Journal of Sex Research · doi:10.1080/00224499.2017.1339774 · Cited by 72 · see citing works
Keverne, E. B., & Kendrick, K. M. (1991) · Brain Research · doi:10.1016/0006-8993(91)90492-e · Cited by 75 · see citing works
Touch Perception Altered by Chronic Pain and by Opioid Blockade
Case, L. K., Čeko, M., Gracely, J. L., Richards, E. A., Olausson, H., & Bushnell, M. C. (2016) · eNeuro · doi:10.1523/eneuro.0138-15.2016 · Cited by 62 · see citing works
“Similar results have been found in studies of a variety of monkey species showing increased solicitation and receipt of grooming after injection of -opioid antagonists (Meller et al., 1980; Fabre-Nys et al., 1982; Schino and Troisi, 1992; Martel et al., 1995; Graves et al., 2002).”
ResultEffects of buprenorphine on responses to social stimuli in healthy adults
Bershad, A. K., Seiden, J. A., & de Wit, H. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.09.011 · Cited by 64 · see citing works
Oliverio, A., Castellano, C., & Puglisi‐Allegra, S. (1984) · International review of neurobiology · doi:10.1016/s0074-7742(08)60682-0 · Cited by 64 · see citing works
Titi Monkeys as a Novel Non-Human Primate Model for the Neurobiology of Pair Bonding .
Bales, K. L., Razo, R. A., Conklin, Q. A., Hartman, S., Mayer, H. S., Rogers, F. D., Simmons, T. C., Smith, L. K., Williams, A. V., Williams, D. R., et al. (2017) · Europe PMC (PubMed Central) · Cited by 62 · see citing works
Opioids and attachment in rhesus macaque (Macaca mulatta) abusive mothers.
Graves, F. C., Wallen, K., & Dario Maestripieri, A. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.3.489 · Cited by 61 · see citing works
“Similar reduction of scratching and self-grooming was also reported by previous studies in which similar doses of naltrexone or naloxone produced no side effects on activity levels (Fabre-Nys et al., 1982; Schino & Troisi, 1992).”
ResultCoping in groups of domestic horses – Review from a social and neurobiological perspective
Dierendonck, M. C. V., & Spruijt, B. M. (2012) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2012.02.007 · Cited by 61 · see citing works
“First, for self-grooming in rats and allo-grooming in primates the effects of opioids have been studied by injecting endorphins and naloxone an opioid antagonist in animals (Fabre-Nys et al., 1982; Schino and Troisi, 1992; Keverne et al., 1997).”
BackgroundSchino, G., & Troisi, A. (1992) · Brain Research · doi:10.1016/0006-8993(92)90617-i · Cited by 61 · see citing works
Oxytocin under opioid antagonism leads to supralinear enhancement of social attention
Dal Monte, O., Piva, M., Anderson, K. M., Tringides, M., Holmes, A. J., & Chang, S. W. C. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1702725114 · Cited by 55 · see citing works
Lloyd, S. A. C., & Dixson, A. F. (1988) · Brain Research · doi:10.1016/0006-8993(88)90405-2 · Cited by 54 · see citing works
Naltrexone alters the processing of social and emotional stimuli in healthy adults
Wardle, M. C., Bershad, A. K., & de Wit, H. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1136355 · Cited by 52 · see citing works
An Individual-Oriented Model on the Emergence of Support in Fights, Its Reciprocation and Exchange
Hemelrijk, C. K., & Puga‐Gonzalez, I. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037271 · Cited by 52 · see citing works
“scratching, yawning and shaking), and increases the level of endorphins in the brain reducing, thus, the motivation to groom; and not being groomed for some length of time reduces the concentration of endorphins and increases the motivation to be groomed [5-7,9,11,12,20-22].”
BackgroundEffects of naloxone on diurnal rhythms in mood and endocrine function: a dose-response study in man
del Campo, A. F. M., Dowson, J. H., Herbert, J., & Paykel, E. S. (1994) · Psychopharmacology · doi:10.1007/bf02244988 · Cited by 52 · see citing works
“Experimental studies have implicated endogenous opioids in the regulation of mood, reproductive hormones and appetite (Olson et al. 1980; Meller et al. 1980; Margules 1984; Fabre-Nys et al. 1982; Herbert 1992).”
BackgroundKendrick, K. M., & Keverne, E. B. (1989) · Brain Research · doi:10.1016/0006-8993(89)91462-5 · Cited by 49 · see citing works
Self-citationAdult Attachment System Links With Brain Mu Opioid Receptor Availability In Vivo.
Turtonen, O., Saarinen, A., Nummenmaa, L., Tuominen, L., Tikka, M., Armio, R., Hautamäki, A., Laurikainen, H., Raitakari, O., Keltikangas-Järvinen, L., et al. (2020) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2020.10.013 · Cited by 81 · see citing works
“This view is supported by pharmacological studies in primates, which have found that opioid antagonist administration increases social grooming in monkeys (72,73), whereas opioid agonists alleviate separation distress in pups (18).”
BackgroundEndogenous opioids: A proximate reward mechanism for kin selection?
D'Amato, F. R., & Pavone, F. (1993) · Behavioral and Neural Biology · doi:10.1016/0163-1047(93)90768-d · Cited by 47 · see citing works
Socio-ecological factors correlate with levels of stereotypic behavior in zoo-housed primates
Pomerantz, O., Meiri, S., & Terkel, J. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.05.005 · Cited by 52 · see citing works
“…has not been groomed for some time, this lowers the level of endorphins in its brain and increases its motivation to be groomed; while, correspondingly, grooming increases the level of endorphins in the brain and alleviates the motivation to groom (Fabre-Nys et al., 1982; Martel et al., 1995).”
BackgroundSocial isolation and social interaction alter regional brain opioid receptor binding in rats
Vanderschuren, L. J. M. J., Stein, E. A., Wiegant, V. M., & van Ree, J. M. (1995) · European Neuropsychopharmacology · doi:10.1016/0924-977x(95)00010-m · Cited by 46 · see citing works
Winslow, J., & Miczek, K. A. (1988) · Psychopharmacology · doi:10.1007/bf02180030 · Cited by 46 · see citing works
Establishment of a preference by the newborn lamb for its mother: The role of opioids.
Shayit, M., Nowak, R., Keller, M., & Weller, A. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.3.446 · Cited by 43 · see citing works
Nocjar, C., & Panksepp, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.04.004 · Cited by 44 · see citing works
Nummenmaa, L., Putkinen, V., & Sams, M. E. (2021) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2021.03.026 · Cited by 41 · see citing works
Social Bonding in the Modulation of the Physiology of Ritual Trance
Frecska, E., & Kulcsár, Z. (1989) · Ethos · doi:10.1525/eth.1989.17.1.02a00040 · Cited by 42 · see citing works
Inagaki, T. K., Hazlett, L. I., & Andreescu, C. (2019) · Journal of Experimental Psychology General · doi:10.1037/xge0000674 · Cited by 38 · see citing works
“Turning to the animal literature, opioid antagonism (vs. placebo) often results in increases, rather than decreases, in social connection behavior (Fabre-Nys et al., 1982; Martel et al., 1995; Schino & Troisi, 1992).”
BackgroundRagen, B. J., Freeman, S. M., Laredo, S. A., Mendoza, S. P., & Bales, K. L. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.023 · Cited by 37 · see citing works
Ragen, B., Maninger, N., Mendoza, S. P., Jarcho, M. R., & Bales, K. L. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.05.009 · Cited by 39 · see citing works
“…talapoin monkeys and macaques, morphine administration decreases the number of grooming solicitations and the amount of grooming received, while naloxone administration increases grooming solicitations and the receipt of grooming (Fabre-Nys et al., 1982; Keverne et al., 1989; Martel et al., 1995).”
InfluentialAffiliative behavior in voles: Effects of morphine, naloxone, and cross-fostering
Shapiro, L. E., Meyer, M. E., & Dewsbury, D. A. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90357-0 · Cited by 37 · see citing works
Smith, C. J. W., Wilkins, K. B., Li, S. J., Tulimieri, M. T., & Veenema, A. H. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.12.017 · Cited by 33 · see citing works
“In both rodents and primates, MOR blockade has been shown to increase the release of the stress hormone cortisol (Fabre-Nys et al., 1982; Jezová et al., 1982; Eisenberg, 1984; Hayes and Stewart, 1985) as well as to increase social comfort-seeking behaviors, such as distress calls and grooming…”
BackgroundMorphine administration selectively facilitates social play in common marmosets*†
Guard, H. J., Newman, J. D., & Roberts, R. L. (2002) · Developmental Psychobiology · doi:10.1002/dev.10043 · Cited by 36 · see citing works
Steklis, H. D., & Kling, A. S. (1985) · Elsevier eBooks · doi:10.1016/b978-0-12-586780-1.50008-2 · Cited by 35 · see citing works
Interplay between the oxytocin and opioid systems in regulating social behaviour
Putnam, P. T., & Chang, S. W. C. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0050 · Cited by 33 · see citing works
“Intramuscular injections of naloxone increased the frequency of social grooming amongst a group of talapoin monkeys, while not effecting aggressive behaviours, rates of self-grooming, or general locomotor movements [117].”
BackgroundPrimate Social Relationships: Their Determinants and Consequences
Keverne, E. B. (1992) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60140-0 · Cited by 34 · see citing works
Kendrick, K. M., & Dixson, A. F. (1986) · Brain Research · doi:10.1016/0006-8993(86)90741-9 · Cited by 32 · see citing works
Martensz, N. D., Vellucci, S. V., Keverne, E. B., & Herbert, J. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90060-6 · Cited by 32 · see citing works
Inoue, K., Burkett, J. P., & Young, L. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.035 · Cited by 31 · see citing works
“Furthermore, in Rhesus macaques, acute administration of an opiate antagonist increases maternal and affiliative behavior, while morphine decreases these behaviors (Fabre-Nys et al., 1982, Kalin et al., 1988, Martel et al., 1993).”
BackgroundLøseth, G. E., Eikemo, M., & Leknes, S. (2019) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsz022 · Cited by 28 · see citing works
Virtual touch and the human social world
Dunbar, R. (2021) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2021.06.009 · Cited by 29 · see citing works
Stoesz, B. M., Hare, J. F., & Snow, W. M. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.11.007 · Cited by 28 · see citing works
Medial amygdala and aggressive behavior: Interaction between testosterone and vasopressin
Koolhaas, J. M., Brink, T. H. C. V. D., Roozendaal, B., & Boorsma, F. (1990) · Aggressive Behavior · doi:10.1002/1098-2337(1990)16:3/4 · Cited by 134 · see citing works
Grandi, L. C. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.01371 · Cited by 23 · see citing works
McMillan, F. D. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.09.013 · Cited by 23 · see citing works
Moods, minds and molecules: the neurochemistry of social behavior
Mench, J. A., & Shea-Moore, M. M. (1995) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(95)00608-u · Cited by 23 · see citing works
Social Influences on Sex Differences in the Behaviour and Endocrine State of Talapoin Monkeys
Keverne, E. B., Eberhart, J. A., Yodyingyuad, U., & Abbott, D. H. (1984) · Progress in brain research · doi:10.1016/s0079-6123(08)64445-3 · Cited by 23 · see citing works
Neurobiology of Social Behavior
Dario Maestripieri, A. (2010) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195326598.003.0019 · Cited by 22 · see citing works
“from other individuals (Fabre-Nys et al., 1982; Keverne et al., 1989; Meller et al., 1980).”
Emergence of complex social networks from spatial structure and rules of thumb: a modelling approach
Puga‐Gonzalez, I., & Sueur, C. (2017) · Ecological Complexity · doi:10.1016/j.ecocom.2017.07.004 · Cited by 22 · see citing works
Sex and Status Effects on Primate Volubility Clues to the Origin of Vocal Languages?
LOCKE, J. L. (1999) · Evolution and Human Behavior · doi:10.1016/s1090-5138(99)00003-3 · Cited by 22 · see citing works
Mu-opioid receptor system modulates responses to vocal bonding and distress signals in humans
Sun, L., Lukkarinen, L., Putkinen, V., Karlsson, H. K., Hirvonen, J., Tiihonen, J., Lauerma, H., Scott, S. K., & Nummenmaa, L. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0181 · Cited by 23 · see citing works
“For instance, in non-human primates, the opioid antagonist naltrexone increases social motivation while decreasing sexual motivation [25,26], while in humans opioid agonists lead to increased social motivation [27].”
BackgroundNeurobiological correlates of defensive behaviors
Bakshi, V. P., Shelton, S. E., & Kalin, N. H. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62133-0 · Cited by 21 · see citing works
Olson, G. A., Olson, R. D., & Kastin, A. J. (1983) · Peptides · doi:10.1016/0196-9781(83)90063-3 · Cited by 21 · see citing works
Rank and relationships in the evolution of spoken language
LOCKE, J. L. (2001) · Journal of the Royal Anthropological Institute · doi:10.1111/1467-9655.00049 · Cited by 20 · see citing works
Hyperstructures and the Biology of Interpersonal Dependence: Rethinking Reciprocity and Altruism
Smith, T. S., & Stevens, G. T. (2002) · Sociological Theory · doi:10.1111/1467-9558.00153 · Cited by 19 · see citing works
Cochlear SGN neurons elevate pain thresholds in response to music
Dunbar, R., Pearce, E., Tarr, B., Makdani, A. D., Bamford, J. S., Smith, S., & McGlone, F. P. (2021) · Scientific Reports · doi:10.1038/s41598-021-93969-0 · Cited by 17 · see citing works
The Central and Peripheral Opioid Peptides: Their Relationships and Functions
Kalin, N. H., & Loevinger, B. L. (1983) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(18)30815-3 · Cited by 18 · see citing works
Social Pleasures of MusicPreprint
Nummenmaa, L., Putkinen, V., & Sams, M. E. (2020) · doi:10.31234/osf.io/y29cd · Cited by 18 · see citing works
“Studies in nonhuman primates suggest a causal role of endogenous opioid receptor (OR) system in modulating social bonding [61,62].”
Pleasurable music activates cerebral µ-opioid receptors: a combined PET-fMRI study
Putkinen, V., Seppälä, K., Harju, H., Hirvonen, J., Karlsson, H. K., & Nummenmaa, L. (2025) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-025-07232-z · Cited by 16 · see citing works
“…social bonding and promote cooperation [20–22], and the involvement of opioids in affiliative behavior, established through pharmacological interventions in non-human primates [23, 24] and PET studies in humans [15, 25], suggests that the MOR systems may mediate these prosocial effects of music.”
Social style and resilience of macaques’ networks, a theoretical investigation
Puga‐Gonzalez, I., Sosa, S., & Sueur, C. (2018) · Primates · doi:10.1007/s10329-018-0684-5 · Cited by 16 · see citing works
Lopez-Vergara, L., Santillán‐Doherty, A. M., Mayagoitia, L., & Mondragón‐Ceballos, R. (1989) · Behavioural Processes · doi:10.1016/s0376-6357(89)80008-7 · Cited by 15 · see citing works
Herbert, J., & Howes, S. R. (1993) · Peptides · doi:10.1016/0196-9781(93)90022-9 · Cited by 15 · see citing works
The Preference for Social Affiliation Renders Fish Willing to Accept Lower O2Levels
Borowiec, B. G., O’Connor, C. M., Goodick, K., Scott, G. R., & Balshine, S. (2017) · Physiological and Biochemical Zoology · doi:10.1086/695566 · Cited by 14 · see citing works
- Authors
- Fabre-Nys, C., Meller, R. E., & Keverne, E. B.
- Affiliations
- University of Cambridge (GB)
- Venue
- Pharmacology Biochemistry and Behavior
- Publisher
- Elsevier BV
- Published
- 1982-04
- Volume
- 16
- Issue
- 4
- Pages
- 653-659
- ISSN
- 0091-3057 (ISSN-L)
- OpenAlex
- W2083065545
- Cited by
- 141
- References
- 38
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 7 · 2021: 6 · 2020: 2 · 2019: 4 · 2018: 2 · 2017: 13 · 2016: 7 · 2015: 6 · 2014: 1 · 2013: 5 · 2012: 4
- FWCI
- 6.17
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Pharmacology Biochemistry and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- Medical Research Council
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- opioid antagonists, naltrexone, naloxone, sulpiride, affiliative behavior, grooming, social bonds, endorphin system, luteinizing hormone, testosterone, cortisol, prolactin, primate social behavior
- MeSH terms
- Animals, Behavior, Animal, Cercopithecidae, Eating, Female, Grooming, Hydrocortisone, Luteinizing Hormone, Male, Motor Activity, Naloxone, Naltrexone, Prolactin, Receptors, Opioid, Social Behavior, Stimulation, Chemical, Sulpiride, Testosterone
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
