The Mu-opioid Receptor and the Evolution of Mother-Infant Attachment: Theoretical Comment on Higham et al. (2011)

Behavioral Neuroscience

Volumn 125, Issue 2, 2011, Pages 273-278

  Curley, James P ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Maternal care; Mother infant attachment; Mu opioid receptor; Opioids; OPRM1

Indexed keywords

BETA ENDORPHIN; DOPAMINE; ESTROGEN; MU OPIATE RECEPTOR; OXYTOCIN; VASOPRESSIN;

AMINO ACID SUBSTITUTION; CHILD PARENT RELATION; EMOTIONAL ATTACHMENT; EVOLUTION; GENE; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; MACACA; MATERNAL BEHAVIOR; MOTHER CHILD RELATION; NONHUMAN; NOTE; NURTURING BEHAVIOR; OPRM1 GENE; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; SOCIAL BEHAVIOR;

ANIMALS; FEMALE; GENETIC VARIATION; MATERNAL BEHAVIOR; OBJECT ATTACHMENT; OXYTOCIN; RECEPTORS, OPIOID, MU;

EID: 79954516999     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0022939     Document Type: Note

References (61)

1. Arvidsson U., Riedl M., Chakrabarti S., Lee J.H., Nakano A.H., Dado R.J., Elde R. Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. Journal of Neuroscience 1995, 15:3328-3341.
2. Bakermans-Kranenburg M.J., van Ijzendoorn M.H. Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting. Soc Cogn Affect Neurosci 2008, 3:128-134.
3. Barr C.S., Chen S.A., Schwandt M.L., Lindell S.G., Sun H., Suomi S.J., Heilig M. Suppression of alcohol preference by naltrexone in the rhesus macaque: A critical role of genetic variation at the micro-opioid receptor gene locus. Biological Psychiatry 2010, 67:78-80.
4. Barr C.S., Schwandt M., Lindell S.G., Chen S.A., Goldman D., Suomi S.J., Heilig M. Association of a functional polymorphism in the mu-opioid receptor gene with alcohol response and consumption in male rhesus macaques Macaca mulatta. Archives of General Psychiatry 2007, 64:369-376.
5. Barr C.S., Schwandt M.L., Lindell S.G., Higley J.D., Maestripieri D., Goldman D., Heilig M. Variation at the mu-opioid receptor gene (OPRM1) influences attachment behavior in infant primates. Proceedings of the National Academy of Sciences, USA 2008, 105:5277-5281.
6. Benoit D. Infant-parent attachment: Definition, types, antecedents, measurement and outcome. Paediatr Child Health 2004, 9:541-545.
7. Bond C., LaForge K.S., Tian M., Melia D., Zhang S., Borg L., Yu L. Single-nucleotide polymorphism in the human mu opioid receptor gene alters beta-endorphin binding and activity: Possible implications for opiate addiction. Proceedings of the National Academy of Sciences, USA 1998, 95(16):9608-9613.
8. Broad K.D., Curley J.P., Keverne E.B. Mother-infant bonding and the evolution of mammalian social relationships. Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences 2006, 361:2199-2214.
9. Broad K.D., Kendrick K.M., Sirinathsinghji D.J., Keverne E.B. Changes in pro-opiomelanocortin and pre-proenkephalin mRNA levels in the ovine brain during pregnancy, parturition and lactation and in response to oestrogen and progesterone. Journal of Neuroendocrinology 1993, 5:711-719.
10. Caba M., Poindron P., Krehbiel D., Levy F., Romeyer A., Venier G. Naltrexone delays the onset of maternal behavior in primiparous parturient ewes. Pharmacology, Biochemistry and Behavior 1995, 52:743-748.
11. Curley J.P., Barton S., Surani A., Keverne E.B. Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proceedings. Biological sciences/The Royal Society 2004, 271:1303-1309.
12. Curley J.P., Keverne E.B. Genes, brains and mammalian social bonds. Trends in Ecology and Evolution 2005, 20:561-567.
13. Dunbar R.I.M. The social role of touch in humans and primates: Behavioural function and neurobiological mechanisms. Neuroscience and Biobehavioral Reviews 2010, 34:260-268.
14. Fields H. State-dependent opioid control of pain. Nature Reviews. Neuroscience 2004, 5:565-575.
15. Franceschini R., Venturini P.L., Cataldi A., Barreca T., Ragni N., Rolandi E. Plasma beta-endorphin concentrations during suckling in lactating women. British Journal of Obstetrics and Gynaecology 1989, 96:711-713.
16. Goodman G., Hans S.L., Cox S.M. Attachment behavior and its antecedents in offspring born to methadone-maintained women. Journal of Clinical Child Psychology 1999, 28:58-69.
17. Gordon K., Hodgen G.D., Richardson D.W. Postpartum lactational anovulation in a nonhuman primate (Macaca fascicularis): endogenous opiate mediation of suckling-induced hyperprolactinemia. Journal of Clinical Endocrinology and Metabolism 1992, 75:59-67.
18. Graves F.C., Wallen K., Maestripieri D. Opioids and attachment in rhesus macaque (Macaca mulatta) abusive mothers. Behavioral Neuroscience 2002, 116:489-493.
19. Herz A. Endogenous opioid systems and alcohol addiction. Psychopharmacology (Berl) 1997, 129:99-111.
20. Higham J.P., Barr C.S., Hoffman C.L., Mandalaywala T.M., Parker K.J., Maestripieri D. Mu-opioid receptor (OPRM1) variation, oxytocin levels and maternal attachment in free-ranging rhesus macaques Macaca mulatta. Behavioral Neuroscience 2011, 125:131-136.
21. Hoffman D.I., Abboud T.K., Haase H.R., Hung T.T., Goebelsmann U. Plasma beta-endorphin concentrations prior to and during pregnancy, in labor, and after delivery. American Journal of Obstetrics and Gynecology 1984, 150:492-496.
22. Kalin N.H., Shelton S.E., Barksdale C.M. Opiate modulation of separation-induced distress in non-human primates. Brain Research 1988, 440:285-292.
23. Kalin N.H., Shelton S.E., Lynn D.E. Opiate systems in mother and infant primates coordinate intimate contact during reunion. Psychoneuroendocrinology 1995, 20:735-742.
24. Kendrick K.M., Keverne E.B. Effects of intracerebroventricular infusions of naltrexone and phentolamine on central and peripheral oxytocin release and on maternal behaviour induced by vaginocervical stimulation in the ewe. Brain Research 1989, 505:329-332.
25. Keverne E.B., Curley J.P. Epigenetics, brain evolution and behaviour. Frontiers in Neuroendocrinology 2008, 29:398-412.
26. Keverne E.B., Kendrick K.M. Morphine and corticotrophin-releasing factor potentiate maternal acceptance in multiparous ewes after vaginocervical stimulation. Brain Research 1991, 540:55-62.
27. Keverne E.B., Martensz N.D., Tuite B. Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology 1989, 14:155-161.
28. Keverne E.B., Nevison C.M., Martel F.L. Early learning and the social bond. Annals of the New York Academy of Sciences 1997, 807:329-339.
29. Kroslak T., Laforge K.S., Gianotti R.J., Ho A., Nielsen D.A., Kreek M.J. The single nucleotide polymorphism A118G alters functional properties of the human mu opioid receptor. Journal of Neurochemistry 2007, 103:77-87.
30. Lejeune C., Ropert J.C., Montamat S., Floch-Tudal C., Mazy F., Wijkhuisen N., Froment H. Devenir médico-social de 59 nouveau-nés de mére toxicomane [Medical-social outcome of 59 infants born to addicted mothers]. Journal de Gynecologie, Obstetrique et Biologie de la Reproduction (Paris) 1997, 26:395-404.
31. Lindow S.W., Hendricks M.S., Nugent F.A., Dunne T.T., van der Spuy Z.M. Morphine suppresses the oxytocin response in breast-feeding women. Gynecologic and Obstetric Investigation 1999, 48:33-37.
32. Lindow S.W., van der Spuy Z.M., Hendricks M.S., Nugent F.A., Dunne T.T. The effect of morphine and naloxone administration on maternal oxytocin concentration in late pregnancy. Clinical Endocrinology (Oxf) 1993, 39:671-675.
33. Lindow S.W., van der Spuy Z.M., Hendricks M.S., Rosselli A.P., Lombard C., Leng G. The effect of morphine and naloxone administration on plasma oxytocin concentrations in the first stage of labour. Clinical Endocrinology (Oxf) 1992, 37:349-353.
34. Maestripieri D. Similarities in affiliation and aggression between cross-fostered rhesus macaque females and their biological mothers. Developmental Psychobiology 2003, 43:321-327.
35. Martel F.L., Nevison C.M., Rayment F.D., Simpson M.J., Keverne E.B. Opioid receptor blockade reduces maternal affect and social grooming in rhesus monkeys. Psychoneuroendocrinology 1993, 18:307-321.
36. Martel F.L., Nevison C.M., Simpson M.J., Keverne E.B. Effects of opioid receptor blockade on the social behavior of rhesus monkeys living in large family groups. Developmental Psychobiology 1995, 28:71-84.
37. McCormack K., Newman T.K., Higley J.D., Maestripieri D., Sanchez M.M. Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Hormones and Behavior 2009, 55:538-547.
38. Mikhail M.S., Youchah J., DeVore N., Ho G.Y., Anyaegbunam A. Decreased maternal-fetal attachment in methadone-maintained pregnant women: A preliminary study. Journal of the Association for Academic Minority Physicians 1995, 6:112-114.
39. Mileva-Seitz V., Kennedy J., Atkinson L., Steiner M., Levitan R., Matthews S.G., Fleming A.S. Serotonin transporter allelic variation in mothers predicts maternal sensitivity, behavior and attitudes toward 6-month-old infants. Genes Brain Behav 2011.
40. Miller G.M., Bendor J., Tiefenbacher S., Yang H., Novak M.A., Madras B.K. A mu-opioid receptor single nucleotide polymorphism in rhesus monkey: Association with stress response and aggression. Molecular Psychiatry 2004, 9:99-108.
41. Misiti A., Turillazzi P.G., Zapponi G.A., Loizzo A. Heroin induces changes in mother-infant monkey communication and subsequent disruption of their dyadic interaction. Pharmacological Research 1991, 24:93-104.
42. Neiderhiser J.M., Reiss D., Pedersen N.L., Lichtenstein P., Spotts E.L., Hansson K., Ellhammer O. Genetic and environmental influences on mothering of adolescents: A comparison of two samples. Developmental Psychology 2004, 40:335-351.
43. Nelson E.E., Panksepp J. Brain substrates of infant-mother attachment: Contributions of opioids, oxytocin, and norepinephrine. Neuroscience and Biobehavioral Reviews 1998, 22:437-452.
44. Nowak R., Goursaud A.P., Levy F., Orgeur P., Schaal B., Belzung C., Uvnas-Moberg K. Cholecystokinin receptors mediate the development of a preference for the mother by newly born lambs. Behavioral Neuroscience 1997, 111:1375-1382.
45. Numan M., Woodside B. Maternity: Neural mechanisms, motivational processes, and physiological adaptations. Behavioral Neuroscience 2010, 124:715-741.
46. Oslin D.W., Berrettini W., Kranzler H.R., Pettinati H., Gelernter J., Volpicelli J.R., O'Brien C.P. A functional polymorphism of the mu-opioid receptor gene is associated with naltrexone response in alcohol-dependent patients. Neuropsychopharmacology 2003, 28:1546-1552.
47. Pang G.S., Wang J., Wang Z., Goh C., Lee C.G. The G allele of SNP E1/A118G at the mu-opioid receptor gene locus shows genomic evidence of recent positive selection. Pharmacogenomics 2009, 10:1101-1109.
48. Ray L.A., Hutchison K.E. A polymorphism of the mu-opioid receptor gene (OPRM1) and sensitivity to the effects of alcohol in humans. Alcoholism, Clinical and Experimental Research 2004, 28:1789-1795.
49. Ray L.A., Hutchison K.E. Effects of naltrexone on alcohol sensitivity and genetic moderators of medication response: A double-blind placebo-controlled study. Archives of General Psychiatry 2007, 64:1069-1077.
50. Schino G., Troisi A. Opiate receptor blockade in juvenile macaques: Effect on affiliative interactions with their mothers and group companions. Brain Research 1992, 576:125-130.
51. Shayit M., Nowak R., Keller M., Weller A. Establishment of a preference by the newborn lamb for its mother: The role of opioids. Behavioral Neuroscience 2003, 117:446-454.
52. Sia A.T., Lim Y., Lim E.C., Goh R.W., Law H.Y., Landau R., Tan E.C. A118G single nucleotide polymorphism of human mu-opioid receptor gene influences pain perception and patient-controlled intravenous morphine consumption after intrathecal morphine for postcesarean analgesia. Anesthesiology 2008, 109:520-526.
53. Simmons D., Self D.W. Role of mu- and delta-opioid receptors in the nucleus accumbens in cocaine-seeking behavior. Neuropsychopharmacology 2009, 34:1946-1957.
54. Thompson R.C., Mansour A., Akil H., Watson S.J. Cloning and pharmacological characterization of a rat mu opioid receptor. Neuron 1993, 11:903-913.
55. Troisi A., Frazzetto G., Carola V., Di Lorenzo G., Coviello M., D'Amato F.R., Gross C. Social hedonic capacity is associated with the A118G polymorphism of the mu-opioid receptor gene (OPRM1) in adult healthy volunteers and psychiatric patients. Social Neuroscience 2010, 6:88-97.
56. van Ijzendoorn M.H., Bakermans-Kranenburg M.J., Mesman J. Dopamine system genes associated with parenting in the context of daily hassles. Genes, Brain, and Behavior 2008, 7:403-410.
57. Vuong C., Van Uum S.H., O'Dell L.E., Lutfy K., Friedman T.C. The effects of opioids and opioid analogs on animal and human endocrine systems. Endocrine Reviews 2010, 31:98-132.
58. Way B.M., Lieberman M.D. Is there a genetic contribution to cultural differences? Collectivism, individualism and genetic markers of social sensitivity. Social Cognitive and Affective Neuroscience 2010, 5:203-211.
59. Way B.M., Taylor S.E., Eisenberger N.I. Variation in the mu-opioid receptor gene (OPRM1) is associated with dispositional and neural sensitivity to social rejection. Proceedings of the National Academy of Sciences, USA 2009, 106:15079-15084.
60. Weller A., Feldman R. Emotion regulation and touch in infants: The role of cholecystokinin and opioids. Peptides 2003, 24:779-788.
61. Zhang Y., Wang D., Johnson A.D., Papp A.C., Sadee W. Allelic expression imbalance of human mu opioid receptor (OPRM1) caused by variant A118G. Journal of Biological Chemistry 2005, 280:32618-32624.