Why social attachment and oxytocin protect against addiction and stress: Insights from the dynamics between ventral and dorsal corticostriatal systems

Pharmacology Biochemistry and Behavior

Volumn 119, Issue , 2014, Pages 39-48

  Tops, Mattie ^a   Koole, Sander L ^a   Ijzerman, Hans ^b   Buisman Pijlman, Femke T A ^c  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b TILBURG UNIVERSITY   (Netherlands)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Addiction; Attachment; Derogation of alternatives; Dopamine; Novelty seeking; Oxytocin

Indexed keywords

DOPAMINE; ENDORPHIN; OXYTOCIN;

ADDICTION; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIOR CONTROL; BEHAVIORAL RESEARCH; CAUDATE NUCLEUS; CHRONIC STRESS; COOPERATION; COPING BEHAVIOR; CORPUS STRIATUM; DRUG ABUSE; DRUG DEPENDENCE; EMOTIONALITY; EXECUTIVE FUNCTION; FEEDBACK SYSTEM; HABITUATION; HIGH RISK BEHAVIOR; HUMAN; LOCOMOTION; LONG TERM MEMORY; MICROTUS OCHROGASTER; MONOGAMY; NEUROBIOLOGY; NEUROMODULATION; NONHUMAN; PAIR BONDING; PREFRONTAL CORTEX; PRIORITY JOURNAL; REWARD; SEROTONINERGIC NERVE CELL; SOCIAL INTERACTION; STRESS; STRIATE CORTEX; SUBSTANTIA NIGRA;

ADDICTION; ATTACHMENT; DEROGATION OF ALTERNATIVES; DOPAMINE; NOVELTY SEEKING; OXYTOCIN;

CEREBRAL CORTEX; CORPUS STRIATUM; HUMANS; OXYTOCIN; SOCIAL BEHAVIOR; SUBSTANCE-RELATED DISORDERS;

EID: 84895535318     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2013.07.015     Document Type: Article

References (108)

1. B.P. Acevedo, A. Aron, H.E. Fisher, and L.L. Brown Neural correlates of long-term intense romantic love Soc Cogn Affect Neurosci 7 2012 145 159
2. M.D. Ainsworth Infant-mother attachment Am Psychol 34 1979 932 937
3. A. Alcaro, and J. Panksepp The SEEKING mind: primal neuro-affective substrates for appetitive incentive states and their pathological dynamics in addictions and depression Neurosci Biobehav Rev 35 2011 1805 1820
4. B.J. Aragona, Y. Liu, Y.J. Yu, J.T. Curtis, J.M. Detwiler, T.R. Insel, and Z. Wang Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds Nat Neurosci 9 2006 133 139
5. A. Aron, H. Fisher, D.J. Mashek, G. Strong, H. Li, and L.L. Brown Reward, motivation, and emotion systems associated with early-stage intense romantic love J Neurophysiol 94 2005 327 337
6. M.J. Bakermans-Kranenburg, and M.H. van Ijzendoorn Differential susceptibility to rearing environment depending on dopamine-related genes: new evidence and a meta-analysis Dev Psychopathol 23 2011 39 52
7. J.A. Barraza, N.S. Grewal, S. Ropacki, P. Perez, A. Gonzalez, and P.J. Zak Effects of a 10-day oxytocin trial in older adults on health and well-being Exp Clin Psychopharmacol 21 2013 85 92
8. A. Bartels, and S. Zeki The neural basis of romantic love Neuroreport 11 2000 3829 3834
9. A. Bartels, and S. Zeki The neural correlates of maternal and romantic love Neuroimage 21 2004 1155 1166
10. J.A. Bartz, J. Zaki, N. Bolger, and K.N. Ochsner Social effects of oxytocin in humans: context and person matter Trends Cogn Sci 15 2011 301 309
11. T.A. Baskerville, and A.J. Douglas Dopamine and oxytocin interactions underlying behaviors: potential contributions to behavioral disorders CNS Neurosci Ther 16 2010 e92 e123
12. L.A. Baxter Dialectical contradictions in relationship development J Soc Pers Relatsh 7 1990 69 88
13. J. Belsky Modern evolutionary theory and patterns of attachment J. Cassidy, P.R. Shaver, Handbook of attachment: theory, research, and clinical applications 1999 Guilford Press New York 141 161
14. K.C. Berridge, and T.E. Robinson Parsing reward Trends Neurosci 26 2003 507 513
15. J. Bick, M. Dozier, K. Bernard, D. Grasso, and R. Simons Foster mother-infant bonding: associations between foster mothers' oxytocin production, electrophysiological brain activity, feelings of commitment, and caregiving quality Child Dev 84 3 2013 826 840
16. F.T.A. Buisman-Pijlman, N.M. Sumracki, J.J. Gordon, P.R. Hull, C.S. Carter, and M. Tops Individual differences underlying susceptibility to addiction: Role for the endogenous oxytocin system Pharmacol Biochem Behav 119 2014 22 38 (this issue)
17. J. Bowlby A secure base: parent-child attachment and healthy human development 1988 Basic Books New York
18. J.P. Burkett, and L.J. Young The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction Psychopharmacology 224 2012 1 26
19. J.P. Burkett, L.L. Spiegel, K. Inoue, A.Z. Murphy, and L.J. Young Activation of mu-opioid receptors in the dorsal striatum is necessary for adult social attachment in monogamous prairie voles Neuropsychopharmacology 36 2011 2200 2210
20. C.S. Carter Oxytocin and sexual behavior Neurosci Biobehav Rev 16 1992 131 144
21. C.S. Carter Neuroendocrine perspectives on social attachment and love Psychoneuroendocrinology 23 1998 779 818
22. C.S. Carter, A.C. DeVries, and L.L. Getz Physiological substrates of mammalian monogamy: the prairie vole model Neurosci Biobehav Rev 19 1995 303 314
23. C.S. Carver, S.L. Johnson, and J. Joormann Serotonergic function, two-mode models of self-regulation, and vulnerability to depression: what depression has in common with impulsive aggression Psychol Bull 134 2008 912 943
24. P.S. Churchland, and P. Winkielman Modulating social behavior with oxytocin: how does it work? What does it mean? Horm Behav 61 2012 392 399
25. M.S. Clark, and E.P. Lemay Jr. Close relationships S.T. Fiske, D.T. Gilbert, G. Lindzey, 5th ed. Handbook of social psychology vol. 2 2010 Wiley New York 898 940
26. M.S. Clark, and J. Mills Interpersonal attraction in exchange and communal relationships J Pers Soc Psychol 37 1 1979 12 24
27. S.M. Clinton, D.M. Vázquez, M. Kabbaj, M.H. Kabbaj, S.J. Watson, and H. Akil Individual differences in novelty-seeking and emotional reactivity correlate with variation in maternal behavior Horm Behav 51 2007 655 664
28. A.R. Cools, and M.A. Gingras Nijmegen high and low responders to novelty: a new tool in the search after the neurobiology of drug abuse liability Pharmacol Biochem Behav 60 1998 151 159
29. M. Corbetta, G. Patel, and G.L. Shulman The reorienting system of the human brain: from environment to theory of mind Neuron 58 2008 306 324
30. K.J.W. Craik The nature of explanation 1943 Cambridge University Press Cambridge
31. B.S. Cushing, and K.M. Kramer Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids Neurosci Biobehav Rev 29 2005 1089 1105
32. C.K. De Dreu Oxytocin modulates cooperation within and competition between groups: an integrative review and research agenda Horm Behav 61 2012 419 428
33. C.H. Declerck, C. Boone, and T. Kiyonari Oxytocin and cooperation under conditions of uncertainty: the modulating role of incentives and social information Horm Behav 57 2010 368 374
34. M. Del Giudice Sex, attachment, and the development of reproductive strategies Behav Brain Sci 32 2009 1 21
35. F. Dellu, P.V. Piazza, W. Mayo, M. Le Moal, and H. Simon Novelty-seeking in rats - biobehavioral characteristics and possible relationship with the sensation-seeking trait in man Neuropsychobiology 34 1996 136 145
36. R.A. Depue, and J.V. Morrone-Strupinsky A neurobehavioral model of affiliative bonding: implications for conceptualizing a human trait of affiliation Behav Brain Sci 28 2005 313 350 [discussion 350-395]
37. A. Di Martino, A. Scheres, D.S. Margulies, A.M. Kelly, L.Q. Uddin, and Z. Shehzad et al. Functional connectivity of human striatum: a resting state FMRI study Cereb Cortex 18 2008 2735 2747
38. E. Dias-Ferreira, J.C. Sousa, I. Melo, P. Morgado, A.R. Mesquita, and J.J. Cerqueira et al. Chronic stress causes frontostriatal reorganization and affects decision-making Science 325 5940 2009 621 625
39. K. Dzirasa, H.W. Phillips, T.D. Sotnikova, A. Salahpour, S. Kumar, and R.R. Gainetdinov et al. Noradrenergic control of cortico-striato-thalamic and mesolimbic cross-structural synchrony J Neurosci 30 2010 6387 6397
40. B.J. Everitt, D. Belin, D. Economidou, Y. Pelloux, J.W. Dalley, and T.W. Robbins Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction Philos Trans R Soc Lond B Biol Sci 363 2008 3125 3135
41. S.E. Fahrbach, J.I. Morrell, and D.W. Pfaff Effect of varying the duration of pre-test cage habituation on oxytocin induction of short-latency maternal behavior Physiol Behav 37 1986 135 139
42. Y. Fan, N.W. Duncan, M. de Greck, and G. Northoff Is there a core neural network in empathy? An fMRI based quantitative meta-analysis Neurosci Biobehav Rev 35 2011 903 911
43. R. Feldman Oxytocin and social affiliation in humans Horm Behav 61 2012 380 391
44. A.P. Fiske The four elementary forms of sociality: framework for a unified theory of social relations Psychol Rev 99 1992 689 723
45. A.R. Furay, and J.F. Neumaier Opioid receptors: binding that ties Neuropsychopharmacology 36 2011 2157 2158
46. G. Gainotti Face familiarity feelings, the right temporal lobe and the possible underlying neural mechanisms Brain Res Rev 56 2007 214 235
47. E.L. Gardner Addiction and brain reward and antireward pathways Adv Psychosom Med 30 2011 22 60
48. C. Grillon, M. Krimsky, D.R. Charney, K. Vytal, M. Ernst, and B. Cornwell Oxytocin increases anxiety to unpredictable threat Mol Psychiatry 2013 10.1038/mp.2012.156 [in press]
49. A.J. Guastella, P.B. Mitchell, and M.R. Dadds Oxytocin increases gaze to the eye region of human faces Biol Psychiatry 63 2008 3 5
50. S.N. Haber, J.L. Fudge, and N.R. McFarland Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum J Neurosci 20 2000 2369 2382
51. M. Häfner, and H. Ijzerman The face of love: spontaneous accommodation as social emotion regulation Pers Soc Psychol Bull 37 2011 1551 1563
52. T.A. Hare, N. Tottenham, M.C. Davidson, G.H. Glover, and B.J. Casey Contributions of amygdala and striatal activity in emotion regulation Biol Psychiatry 57 2005 624 632
53. J.J. Heisz, and J.D. Ryan The effects of prior exposure on face processing in younger and older adults Front Aging Neurosci 3 2011 15
54. C.M. Hostetler, S.L. Harkey, T.B. Krzywosinski, B.J. Aragona, and K.L. Bales Neonatal exposure to the D1 agonist SKF38393 inhibits pair bonding in the adult prairie vole Behav Pharmacol 22 2011 703 710
55. R.H. Hoyle, M.C. Fejfar, and J.D. Miller Personality and sexual risk taking: a quantitative review J Pers 68 2000 1203 1231
56. T.R. Insel Is social attachment an addictive disorder? Physiol Behav 79 2003 351 357
57. S. Jahfari, L. Waldorp, W.P. van den Wildenberg, H.S. Scholte, K.R. Ridderinkhof, and B.U. Forstmann Effective connectivity reveals important roles for both the hyperdirect (fronto-subthalamic) and the indirect (fronto-striatal-pallidal) fronto-basal ganglia pathways during response inhibition J Neurosci 31 2011 6891 6899
58. D. Joel, and I. Weiner The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum Neuroscience 96 2000 451 474
59. P.N. Johnson-Laird Mental models 1983 Harvard University Press Cambridge, MA
60. A.E. Kelley, T. Schochet, and C.F. Landry Risk taking and novelty seeking in adolescence: introduction to part I Ann N Y Acad Sci 1021 2004 27 32
61. J. Klackl, M. Pfundmair, D. Agroskin, and E. Jonas Who's to blame? Oxytocin promotes nonpersonalistic attributions in response to a trust betrayal Biol Psychol 92 2012 387 394
62. G.F. Koob, and N.D. Volkow Neurocircuitry of addiction Neuropsychopharmacology 35 2010 217 238
63. M.J. Kreek, D.A. Nielsen, E.R. Butelman, and K.S. LaForge Genetic influences on impulsivity, risk taking, stress responsivity and vulnerability to drug abuse and addiction Nat Neurosci 8 2005 1450 1457
64. K.W. Lee, Y. Kim, A.M. Kim, K. Helmin, A.C. Nairn, and P. Greengard Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens Proc Natl Acad Sci U S A 103 2006 3399 3404
65. Y. Liu, and Z.X. Wang Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles Neuroscience 121 2003 537 544
66. Y. Liu, B.J. Aragona, K.A. Young, D.M. Dietz, M. Kabbaj, and M. Mazei-Robison et al. Nucleus accumbens dopamine mediates amphetamine-induced impairment of social bonding in a monogamous rodent species Proc Natl Acad Sci U S A 107 2010 1217 1222
67. Y. Liu, K.A. Young, J.T. Curtis, B.J. Aragona, and Z. Wang Social bonding decreases the rewarding properties of amphetamine through a dopamine D1 receptor-mediated mechanism J Neurosci 31 2011 7960 7966
68. I.S. McGregor, and M.T. Bowen Breaking the loop: oxytocin as a potential treatment for drug addiction Horm Behav 61 2012 331 339
69. M.L. Meyer, E.T. Berkman, J.C. Karremans, and M.D. Lieberman Incidental regulation of attraction: the neural basis of the derogation of attractive alternatives in romantic relationships Cogn Emotion 25 2011 490 505
70. M.R. Munafò, B. Yalcin, S.A. Willis-Owen, and J. Flint Association of the dopamine D4 receptor (DRD4) gene and approach-related personality traits: meta-analysis and new data Biol Psychiatry 63 2008 197 206
71. S. Ortigue, F. Bianchi-Demicheli, N. Patel, C. Frum, and J.W. Lewis Neuroimaging of love: fMRI meta-analysis evidence toward new perspectives in sexual medicine J Sex Med 7 2010 3541 3552
72. J. Panksepp, E. Nelson, and M. Bekkedal Brain systems for the mediation of social separation-distress and social-reward. Evolutionary antecedents and neuropeptide intermediaries Ann N Y Acad Sci 807 1997 78 100
73. C.A. Pedersen How love evolved from sex and gave birth to intelligence and human nature J Bioecon 6 2004 39 63
74. P. Petrovic, R. Kalisch, T. Singer, and R.J. Dolan Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity J Neurosci 28 2008 6607 6615
75. J.G. Pfaus Pathways of sexual desire J Sex Med 6 2009 1506 1533
76. M.L. Phillips, W.C. Drevets, S.L. Rauch, and R. Lane Neurobiology of emotion perception II: implications for major psychiatric disorders Biol Psychiatry 54 2003 515 528
77. P.V. Piazza, F. Rougé-Pont, V. Deroche, S. Maccari, H. Simon, and M. Le Moal Glucocorticoids have state-dependent stimulant effects on the mesencephalic dopaminergic transmission Proc Natl Acad Sci U S A 93 1996 8716 8720
78. F. Pijlman, A.H.J. Herremans, J. Van de Kieft, C.G. Kruse, and J. Van Ree Prepulse inhibition of startle increased and startle reflex decreased after chronic mild physical, but not emotional stress in the rat Eur Neuropsychopharmacol 13 2003 369 380
79. C.J. Pilkington Perceptions of risk in intimacy J Soc Pers Relatsh 5 1988 503 508
80. J.K. Rilling, A.C. Demarco, P.D. Hackett, R. Thompson, B. Ditzen, and R. Patel et al. Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men Psychoneuroendocrinology 37 2012 447 461
81. C.E. Rusbult, and B.P. Buunk Commitment processes in close relationships: an interdependence analysis J Soc Pers Relatsh 10 1993 175 204
82. V.A. Russell, R. Allin, M.C. Lamm, and J.J. Taljaard Regional distribution of monoamines and dopamine D1- and D2-receptors in the striatum of the rat Neurochem Res 17 1992 387 395
83. Z. Sarnyai, and G.L. Kovács Role of oxytocin in the neuroadaptation to drugs of abuse Psychoneuroendocrinology 19 1994 85 117
84. D. Scheele, N. Striepens, O. Güntürkün, S. Deutschländer, W. Maier, and K.M. Kendrick et al. Oxytocin modulates social distance between males and females J Neurosci 32 2012 16074 16079
85. L. Schwabe, A. Dickinson, and O.T. Wolf Stress, habits, and drug addiction: a psychoneuroendocrinological perspective Exp Clin Psychopharmacol 19 2011 53 63
86. S.M. Siviy Neurobiological substrates of play behavior: glimpses into the structure and function of mammalian playfulness M. Bekoff, J.A. Byers, Animal play: evolutionary, comparative, and ecological perspectives 1998 Cambridge University Press Cambridge
87. A.S. Smith, and Z. Wang Salubrious effects of oxytocin on social stress-induced deficits Horm Behav 61 2012 320 330
88. D.J. Stein, and B. Vythilingum Love and attachment: the psychobiology of social bonding CNS Spectr 14 2009 239 242
89. N. Striepens, D. Scheele, K.M. Kendrick, B. Becker, L. Schäfer, and K. Schwalba et al. Oxytocin facilitates protective responses to aversive social stimuli in males Proc Natl Acad Sci U S A 109 2012 18144 18149
90. S.C. Tanaka, N. Schweighofer, S. Asahi, K. Shishida, Y. Okamoto, and S. Yamawaki et al. Serotonin differentially regulates short- and long-term prediction of rewards in the ventral and dorsal striatum PLoS One 2 2007 e1333
91. S.F. Taylor, and I. Liberzon Neural correlates of emotion regulation in psychopathology Trends Cogn Sci 11 2007 413 418
92. M. Tops Are the insular cortex and cortisol implicated in Parkinsonian features? Parkinsonism Relat Disord 12 8 2006 467 471
93. M. Tops, and M.A.S. Boksem Absorbed in the task: personality measures predict engagement during task performance as tracked by error negativity and asymmetrical frontal activity Cogn Affect Behav Neurosci 10 2010 441 453
94. M. Tops, and M.A.S. Boksem A potential role of the inferior frontal gyrus and anterior insula in cognitive control, brain rhythms and event-related potentials Front Psychol 2 330 2011 1 14
95. M. Tops, and M.A.S. Boksem "What's that?" "What went wrong?" Positive and negative surprise and the rostral-ventral to caudal-dorsal functional gradient in the brain Front Psychol 3 21 2012 1 5
96. M. Tops, A.A. Wijers, T. Koch, and J. Korf Modulation of rotational behavior in healthy volunteers by cortisol administration Biol Psychol 71 2006 240 243
97. M. Tops, S. Russo, M.A. Boksem, and D.M. Tucker Serotonin: modulator of a drive to withdraw Brain Cogn 71 2009 427 436
98. M. Tops, M.A.S. Boksem, P. Luu, and D.M. Tucker Brain substrates of behavioral programs associated with self-regulation Front Psychol 1 152 2010 1 14
99. M. Tops, P. Luu, M.A.S. Boksem, and D.M. Tucker The roles of reactive and prospective behavioral/physiological programs in resilience M. Kent, M.C. Davis, J.W. Reich, The resilience handbook: approaches to stress and trauma 2013 Routledge Publishers New York
100. M. Tops, F.T.A. Buisman-Pijlman, and C.S. Carter Oxytocin and attachment facilitate a shift from seeking novelty to recognizing and preferring familiarity: the key to increasing resilience? M. Kent, M.C. Davis, J.W. Reich, The resilience handbook: approaches to stress and trauma 2013 Routledge Publishers New York
101. D.M. Tucker, and P. Luu Neurophysiology of motivated learning: adaptive mechanisms of cognitive bias in depression Cogn Ther Res 31 2007 189 209
102. K. Uvnäs-Moberg Oxytocin may mediate the benefits of positive social interaction and emotions Psychoneuroendocrinology 23 1998 819 835
103. K. Uvnäs-Moberg, E. Björkstrand, V. Hillegaart, and S. Ahlenius Oxytocin as a possible mediator of SSRI-induced antidepressant effects Psychopharmacology 142 1999 95 101
104. D.A. White, M. Kalinichev, and S.G. Holtzman Locomotor response to novelty as a predictor of reactivity to aversive stimuli in the rat Brain Res 1149 2007 141 148
105. D. Wittfoth-Schardt, J. Gründing, M. Wittfoth, H. Lanfermann, M. Heinrichs, and G. Domes et al. Oxytocin modulates neural reactivity to children's faces as a function of social salience Neuropsychopharmacology 37 2012 1799 1807
106. M. Yoshida, Y. Takayanagi, K. Inoue, T. Kimura, L.J. Young, and T. Onaka et al. Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice J Neurosci 29 2009 2259 2271
107. L.J. Young, Z. Wang, and T.R. Insel Neuroendocrine bases of monogamy Trends Neurosci 21 1998 71 75
108. K.A. Young, K.L. Gobrogge, and Z. Wang The role of mesocorticolimbic dopamine in regulating interactions between drugs of abuse and social behavior Neurosci Biobehav Rev 35 2011 498 515