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The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction

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Abstract

Rationale

Love has long been referred to as an addiction in literature and poetry. Scientists have often made comparisons between social attachment processes and drug addiction, and it has been suggested that the two may share a common neurobiological mechanism. Brain systems that evolved to govern attachments between parents and children and between monogamous partners may be the targets of drugs of abuse and serve as the basis for addiction processes.

Objectives

Here, we review research on drug addiction in parallel with research on social attachments, including parent–offspring attachments and social bonds between mating partners. This review focuses on the brain regions and neurochemicals with the greatest overlap between addiction and attachment and, in particular, the mesolimbic dopamine (DA) pathway.

Results

Significant overlap exists between these two behavioral processes. In addition to conceptual overlap in symptomatology, there is a strong commonality between the two domains regarding the roles and sites of action of DA, opioids, and corticotropin-releasing factor. The neuropeptides oxytocin and vasopressin are hypothesized to integrate social information into attachment processes that is not present in drug addiction.

Conclusions

Social attachment may be understood as a behavioral addiction, whereby the subject becomes addicted to another individual and the cues that predict social reward. Understandings from both fields may enlighten future research on addiction and attachment processes.

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References

  • Acevedo BP, Aron A, Fisher HE, Brown LL (2012) Neural correlates of long-term intense romantic love. Soc Cogn Affect Neurosci 7:145–159

    Article  PubMed  Google Scholar 

  • Agmo A, Berenfeld R (1990) Reinforcing properties of ejaculation in the male rat: role of opioids and dopamine. Behav Neurosci 104:177–182

    Article  PubMed  CAS  Google Scholar 

  • Ahern TH, Modi ME, Burkett JP, Young LJ (2009) Evaluation of two automated metrics for analyzing partner preference tests. J Neurosci Meth 182:180–188

    Article  Google Scholar 

  • Ahern TH, Hammock EAD, Young LJ (2011) Parental division of labor, coordination, and the effects of family structure on parenting in monogamous prairie voles (Microtus ochrogaster). Dev Psychobiol 53:118–131

    Article  PubMed  Google Scholar 

  • Alonso G, Szafarczyk A, Assenmacher I (1986) Radioautographic evidence that axons from the area of supraoptic nuclei in the rat project to extrahypothalamic brain regions. Neurosci Lett 66:251–256

    Article  PubMed  CAS  Google Scholar 

  • Altshuler HL, Phillips PE, Feinhandler DA (1980) Alteration of ethanol self-administration by naltrexone. Life Sci 26:679–688

    Article  PubMed  CAS  Google Scholar 

  • American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders: DSM-IV-TR. American Psychiatric Association, Washington, DC

    Google Scholar 

  • American Psychiatric Association DSM-5 Development (2012) Substance use and addictive disorders. Available at http://www.dsm5.org. Accessed 6 June 2012

  • Andari E, Duhamel JR, Zalla T, Herbrecht E, Leboyer M, Sirigu A (2010) Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proc Natl Acad Sci U S A 107:4389–4394

    Article  PubMed  CAS  Google Scholar 

  • Anderson SM, Pierce RC (2005) Cocaine-induced alterations in dopamine receptor signaling: implications for reinforcement and reinstatement. Pharmacol Ther 106:389–403

    Article  PubMed  CAS  Google Scholar 

  • Anderson SM, Famous KR, Sadri-Vakili G, Kumaresan V, Schmidt HD, Bass CE, Terwilliger EF, Cha JH, Pierce RC (2008) Camkii: a biochemical bridge linking accumbens dopamine and glutamate systems in cocaine seeking. Nat Neurosci 11:344–353

    Article  PubMed  CAS  Google Scholar 

  • Aragona BJ, Wang Z (2009) Dopamine regulation of social choice in a monogamous rodent species. Front Behav Neurosci 3:15

    Article  PubMed  CAS  Google Scholar 

  • Aragona BJ, Liu Y, Curtis JT, Stephan FK, Wang Z (2003) A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles. J Neurosci 23:3483–3490

    PubMed  CAS  Google Scholar 

  • Aragona BJ, Liu Y, Yu YJ, Curtis JT, Detwiler JM, Insel TR, Wang Z (2006) Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nat Neurosci 9:133–139

    Article  PubMed  CAS  Google Scholar 

  • Archer R (1974) Chemistry of the neurohypophyseal hormones: an example of molecular evolution. In: Sawyer W, Knobil E (eds) Handbook of physiology. American Physiological Society, Washington, DC, pp 119–130

    Google Scholar 

  • Aron A, Fisher H, Mashek DJ, Strong G, Li H, Brown LL (2005) Reward, motivation, and emotion systems associated with early-stage intense romantic love. J Neurophysiol 94:327–337

    Article  PubMed  Google Scholar 

  • Bachtell RK, Whisler K, Karanian D, Self DW (2005) Effects of intra-nucleus accumbens shell administration of dopamine agonists and antagonists on cocaine-taking and cocaine-seeking behaviors in the rat. Psychopharmacol (Berl) 183:41–53

    Article  CAS  Google Scholar 

  • Bakermans-Kranenburg MJ, van Ijzendoorn MH (2007) Research review: genetic vulnerability or differential susceptibility in child development: the case of attachment. J Child Psychol Psychiatry 48:1160–1173

    Article  PubMed  Google Scholar 

  • Bale TL, Vale WW (2004) CRF and CRF receptors: role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 44:525–557

    Article  PubMed  CAS  Google Scholar 

  • Baracz SJ, Rourke PI, Pardey MC, Hunt GE, McGregor IS, Cornish JL (2012) Oxytocin directly administered into the nucleus accumbens core or subthalamic nucleus attenuates methamphetamine-induced conditioned place preference. Behav Brain Res 228:185–193

    Article  PubMed  CAS  Google Scholar 

  • Barr CS, Schwandt M, Lindell SG, Chen SA, Goldman D, Suomi SJ, Higley JD, Heilig M (2007) Association of a functional polymorphism in the mu-opioid receptor gene with alcohol response and consumption in male rhesus macaques. Arch Gen Psychiatry 64:369–376

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bartels A, Zeki S (2000) The neural basis of romantic love. NeuroReport 11:3829–3834

    Article  PubMed  CAS  Google Scholar 

  • Bedier J, Belloc H (2004) The romance of Tristan and Iseult. Dover, Mineola

    Google Scholar 

  • Beninger RJ, Cheng M, Hahn BL, Hoffman DC, Mazurski EJ, Morency MA, Ramm P, Stewart RJ (1987) Effects of extinction, pimozide, SCH 23390, and metoclopramide on food-rewarded operant responding of rats. Psychopharmacol (Berl) 92:343–349

    Article  CAS  Google Scholar 

  • Beninger RJ, Hoffman DC, Mazurski EJ (1989) Receptor subtype-specific dopaminergic agents and conditioned behavior. Neurosci Biobehav Rev 13:113–122

    Article  PubMed  CAS  Google Scholar 

  • Berridge KC (2007) The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacol (Berl) 191:391–431

    Article  CAS  Google Scholar 

  • Bertran-Gonzalez J, Bosch C, Maroteaux M, Matamales M, Herve D, Valjent E, Girault JA (2008) Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 28:5671–5685

    Article  PubMed  CAS  Google Scholar 

  • Bielsky IF, Young LJ (2004) Oxytocin, vasopressin, and social recognition in mammals. Peptides 25:1565–1574

    Article  PubMed  CAS  Google Scholar 

  • Bielsky IF, Hu SB, Szegda KL, Westphal H, Young LJ (2004) Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacol 29:483–493

    Article  CAS  Google Scholar 

  • Bielsky IF, Hu SB, Ren X, Terwilliger EF, Young LJ (2005) The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47:503–513

    Article  PubMed  CAS  Google Scholar 

  • Birdsall NJ, Hulme EC (1976) C fragment of lipotropin has a high affinity for brain opiate receptors. Nature 260:793–795

    Article  PubMed  CAS  Google Scholar 

  • Blackburn JR, Pfaus JG, Phillips AG (1992) Dopamine functions in appetitive and defensive behaviours. Prog Neurobiol 39:247–279

    Article  PubMed  CAS  Google Scholar 

  • Blacktop JM, Seubert C, Baker DA, Ferda N, Lee G, Graf EN, Mantsch JR (2011) Augmented cocaine seeking in response to stress or CRF delivered into the ventral tegmental area following long-access self-administration is mediated by CRF receptor type 1 but not CRF receptor type 2. J Neurosci 31:11396–11403

    Article  PubMed  CAS  Google Scholar 

  • Borrow AP, Cameron NM (2012) The role of oxytocin in mating and pregnancy. Horm Behav 61:266–276

    Article  PubMed  CAS  Google Scholar 

  • Bosch OJ, Nair HP, Ahern TH, Neumann ID, Young LJ (2009) The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent. Neuropsychopharmacol 34:1406–1415

    Article  CAS  Google Scholar 

  • Bradberry JC, Raebel MA (1981) Continuous infusion of naloxone in the treatment of narcotic overdose. Drug Intell Clin Pharm 15:945–950

    PubMed  CAS  Google Scholar 

  • Briand LA, Flagel SB, Seeman P, Robinson TE (2008) Cocaine self-administration produces a persistent increase in dopamine D2 high receptors. Eur Neuropsychopharmacol 18:551–556

    Article  PubMed  CAS  Google Scholar 

  • Broekkamp CL, Phillips AG (1979) Facilitation of self-stimulation behavior following intracerebral microinjections of opioids into the ventral tegmental area. Pharmacol Biochem Behav 11:289–295

    Article  PubMed  CAS  Google Scholar 

  • Brown R, Dewan S (2009) Mysteries Remain after Governor Admits an Affair. The New York Times, June 24, 2009

  • Bruijnzeel AW (2009) Kappa-opioid receptor signaling and brain reward function. Brain Res Rev 62:127–146

    Article  PubMed  CAS  Google Scholar 

  • Buckholtz JW, Treadway MT, Cowan RL, Woodward ND, Li R, Ansari MS, Baldwin RM, Schwartzman AN, Shelby ES, Smith CE, Kessler RM, Zald DH (2010) Dopaminergic network differences in human impulsivity. Science 329:532

    Article  PubMed  CAS  Google Scholar 

  • Buckley PF (1999) The role of typical and atypical antipsychotic medications in the management of agitation and aggression. Journal of Clin Psychiatry 60:52–60

    Google Scholar 

  • Buijs RM, De Vries GJ, Van Leeuwen FW, Swaab DF (1983) Vasopressin and oxytocin: distribution and putative functions in the brain. Prog Brain Res 60:115–122

    Article  PubMed  CAS  Google Scholar 

  • Burbach JP, Young LJ, Russell J (2005) Oxytocin: synthesis, secretion, and reproductive functions. In: Neill JD (ed) Knobil and Neill's physiology of reproduction. Academic, New York, pp 3055–3127

    Google Scholar 

  • Burkett JP, Spiegel LL, Inoue K, Murphy AZ, Young LJ (2011) Activation of μ-opioid receptors in the dorsal striatum is necessary for adult social attachment in monogamous prairie voles. Neuropsychopharmacol 36:2200–2210

    Article  CAS  Google Scholar 

  • Burns DL, Hewlett EL, Moss J, Vaughan M (1983) Pertussis toxin inhibits enkephalin stimulation of GTPase of NG108-15 cells. J Biol Chem 258:1435–1438

    PubMed  CAS  Google Scholar 

  • Caldwell HK, Lee HJ, Macbeth AH, Young WS 3rd (2008) Vasopressin: behavioral roles of an "original" neuropeptide. Prog Neurobiol 84:1–24

    Article  PubMed  CAS  Google Scholar 

  • Carmichael MS, Humbert R, Dixen J, Palmisano G, Greenleaf W, Davidson JM (1987) Plasma oxytocin increases in the human sexual-response. J Clin Endocrinol Metab 64:27–31

    Article  PubMed  CAS  Google Scholar 

  • Carson DS, Cornish JL, Guastella AJ, Hunt GE, McGregor IS (2010a) Oxytocin decreases methamphetamine self-administration, methamphetamine hyperactivity, and relapse to methamphetamine-seeking behaviour in rats. Neuropharmacology 58:38–43

    Article  PubMed  CAS  Google Scholar 

  • Carson DS, Hunt GE, Guastella AJ, Barber L, Cornish JL, Arnold JC, Boucher AA, McGregor IS (2010b) Systemically administered oxytocin decreases methamphetamine activation of the subthalamic nucleus and accumbens core and stimulates oxytocinergic neurons in the hypothalamus. Addict Biol 15:448–463

    Article  PubMed  CAS  Google Scholar 

  • Carter CS, Roberts RL (1997) The psychobiological basis of cooperative breeding in rodents. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge

    Google Scholar 

  • Carter CS, DeVries AC, Getz LL (1995) Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci Biobehav Rev 19:303–314

    Article  PubMed  CAS  Google Scholar 

  • Champagne F, Diorio J, Sharma S, Meaney MJ (2001) Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci U S A 98:12736–12741

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Mestek A, Liu J, Hurley JA, Yu L (1993) Molecular cloning and functional expression of a mu-opioid receptor from rat brain. Mol Pharmacol 44:8–12

    PubMed  CAS  Google Scholar 

  • Chen YW, Rada PV, Butzler BP, Leibowitz SF, Hoebel BG (2012) Corticotropin-releasing factor in the nucleus accumbens shell induces swim depression, anxiety, and anhedonia along with changes in local dopamine/acetylcholine balance. Neuroscience 206:155–166

    Article  PubMed  CAS  Google Scholar 

  • Christensson K, Nilsson BA, Stock S, Matthiesen AS, Uvnasmoberg K (1989) Effect of nipple stimulation on uterine activity and on plasma-levels of oxytocin in full term, healthy, pregnant-women. Acta Obstetricia Et Gynecologica Scandinavica 68:205–210

    Article  PubMed  CAS  Google Scholar 

  • Claytor R, Lile JA, Nader MA (2006) The effects of eticlopride and the selective D3-antagonist PNU 99194-A on food- and cocaine-maintained responding in rhesus monkeys. Pharmacol Biochem Behav 83:456–464

    Article  PubMed  CAS  Google Scholar 

  • Cooney NL, Litt MD, Morse PA, Bauer LO, Gaupp L (1997) Alcohol cue reactivity, negative-mood reactivity, and relapse in treated alcoholic men. J Abnorm Psychol 106:243–250

    Article  PubMed  CAS  Google Scholar 

  • Cooper BR, Breese GR (1975) A role for dopamine in the psychopharmacology of electrical self-stimulation of the lateral hypothalamus, substantia nigra, and locus coeruleus. Psychopharmacol Bull 11:30–31

    PubMed  CAS  Google Scholar 

  • Corrigall WA, Coen KM, Adamson KL, Chow BL, Zhang J (2000) Response of nicotine self-administration in the rat to manipulations of mu-opioid and gamma-aminobutyric acid receptors in the ventral tegmental area. Psychopharmacol (Berl) 149:107–114

    Article  CAS  Google Scholar 

  • Couppis MH, Kennedy CH (2008) The rewarding effect of aggression is reduced by nucleus accumbens dopamine receptor antagonism in mice. Psychopharmacology (Berl) 197:449–456

    Article  CAS  Google Scholar 

  • Curley JP (2011) The mu-opioid receptor and the evolution of mother-infant attachment: theoretical comment on higham et al. Behav Neurosci 125:273–278

    Article  PubMed  Google Scholar 

  • Curran EJ, Watson SJ Jr (1995) Dopamine receptor mRNA expression patterns by opioid peptide cells in the nucleus accumbens of the rat: a double in situ hybridization study. J Comp Neurol 361:57–76

    Article  PubMed  CAS  Google Scholar 

  • Curtis JT, Wang Z (2007) Amphetamine effects in microtine rodents: a comparative study using monogamous and promiscuous vole species. Neuroscience 148:857–866

    Article  PubMed  CAS  Google Scholar 

  • Curtis JT, Liu Y, Aragona BJ, Wang Z (2006) Dopamine and monogamy. Brain Res 1126:76–90

    Article  PubMed  CAS  Google Scholar 

  • Damsma G, Pfaus JG, Wenkstern D, Phillips AG, Fibiger HC (1992) Sexual behavior increases dopamine transmission in the nucleus accumbens and striatum of male rats: comparison with novelty and locomotion. Behav Neurosci 106:181–191

    Article  PubMed  CAS  Google Scholar 

  • Dantzer R, Bluthe RM, Koob GF, Le Moal M (1987) Modulation of social memory in male rats by neurohypophyseal peptides. Psychopharmacology (Berl) 91:363–368

    Article  CAS  Google Scholar 

  • Daunais JB, Roberts DC, McGinty JF (1993) Cocaine self-administration increases preprodynorphin, but not c-fos, mRNA in rat striatum. NeuroReport 4:543–546

    Article  PubMed  CAS  Google Scholar 

  • De Vry J, Donselaar I, Van Ree JM (1989) Food deprivation and acquisition of intravenous cocaine self-administration in rats: effect of naltrexone and haloperidol. J Pharmacol Exp Ther 251:735–740

    PubMed  Google Scholar 

  • de Wit H, Stewart J (1981) Reinstatement of cocaine-reinforced responding in the rat. Psychopharmacology (Berl) 75:134–143

    Article  Google Scholar 

  • Deroche-Gamonet V, Belin D, Piazza PV (2004) Evidence for addiction-like behavior in the rat. Science 305:1014–1017

    Article  PubMed  CAS  Google Scholar 

  • DeVries AC, DeVries MB, Taymans SE, Carter CS (1996) The effects of stress on social preferences are sexually dimorphic in prairie voles. Proc Natl Acad Sci U S A 93:11980–11984

    Article  PubMed  CAS  Google Scholar 

  • DeVries AC, Guptaa T, Cardillo S, Cho M, Carter CS (2002) Corticotropin-releasing factor induces social preferences in male prairie voles. Psychoneuroendocrinology 27:705–714

    Article  PubMed  CAS  Google Scholar 

  • Di Chiara G, Imperato A (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci U S A 85:5274–5278

    Article  PubMed  Google Scholar 

  • Di Chiara G, Bassareo V, Fenu S, De Luca MA, Spina L, Cadoni C, Acquas E, Carboni E, Valentini V, Lecca D (2004) Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47(Suppl 1):227–241

    Article  PubMed  CAS  Google Scholar 

  • Dichiara G, Imperato A (1988) Opposite effects of mu-opiate and kappa-opiate agonists on dopamine release in the nucleus accumbens and in the dorsal caudate of freely moving rats. J Pharmacol Exp Ther 244:1067–1080

    CAS  Google Scholar 

  • Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC (2007) Oxytocin improves "mind-reading" in humans. Biol Psychiatry 61:731–733

    Article  PubMed  CAS  Google Scholar 

  • Donaldson ZR, Young LJ (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322:900–904

    Article  PubMed  CAS  Google Scholar 

  • Drevets WC, Gautier C, Price JC, Kupfer DJ, Kinahan PE, Grace AA, Price JL, Mathis CA (2001) Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria. Biol Psychiatry 49:81–96

    Article  PubMed  CAS  Google Scholar 

  • Dreyer JK, Herrik KF, Berg RW, Hounsgaard JD (2010) Influence of phasic and tonic dopamine release on receptor activation. J Neurosci 30:14273–14283

    Article  PubMed  CAS  Google Scholar 

  • Dumont GJ, Sweep FC, van der Steen R, Hermsen R, Donders AR, Touw DJ, van Gerven JM, Buitelaar JK, Verkes RJ (2009) Increased oxytocin concentrations and prosocial feelings in humans after ecstasy (3,4-methylenedioxymethamphetamine) administration. Soc Neurosci 4:359–366

    Article  PubMed  CAS  Google Scholar 

  • Dunn AJ, Berridge CW (1990) Physiological and behavioral responses to corticotropin-releasing factor administration: is CRF a mediator of anxiety or stress responses? Brain Res Brain Res Rev 15:71–100

    Article  PubMed  CAS  Google Scholar 

  • El Daly E, Chefer V, Sandill S, Shippenberg TS (2000) Modulation of the neurotoxic effects of methamphetamine by the selective kappa-opioid receptor agonist U69593. J Neurochem 74:1553–1562

    Article  PubMed  CAS  Google Scholar 

  • Evans CJ, Keith DE Jr, Morrison H, Magendzo K, Edwards RH (1992) Cloning of a delta opioid receptor by functional expression. Science 258:1952–1955

    Article  PubMed  CAS  Google Scholar 

  • Everitt BJ, Robbins TW (2000) Second-order schedules of drug reinforcement in rats and monkeys: measurement of reinforcing efficacy and drug-seeking behaviour. Psychopharmacology (Berl) 153:17–30

    Article  CAS  Google Scholar 

  • Fahrbach SE, Morrell JI, Pfaff DW (1985) Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40:526–532

    Article  PubMed  CAS  Google Scholar 

  • Fehr C, Yakushev I, Hohmann N, Buchholz HG, Landvogt C, Deckers H, Eberhardt A, Klager M, Smolka MN, Scheurich A, Dielentheis T, Schmidt LG, Rosch F, Bartenstein P, Grunder G, Schreckenberger M (2008) Association of low striatal dopamine D2 receptor availability with nicotine dependence similar to that seen with other drugs of abuse. Am J Psychiatry 165:507–514

    Article  PubMed  Google Scholar 

  • Feldman R (2012) Oxytocin and social affiliation in humans. Horm Behav 61:380–391

    Article  PubMed  CAS  Google Scholar 

  • Ferguson JN, Young LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25:284–288

    Article  PubMed  CAS  Google Scholar 

  • Ferguson JN, Aldag JM, Insel TR, Young LJ (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21:8278–8285

    PubMed  CAS  Google Scholar 

  • Fisher HE (2004) Why we love: the nature and chemistry of romantic love. H. Holt, New York

    Google Scholar 

  • Freeman SM, Young LJ (2012) Oxytocin, vasopressin, and the evolution of monogamy in mammals. In: Choleris E, Pfaff DW (eds) Oxytocin and vasopressin. Cambridge University Press, Cambridge

    Google Scholar 

  • Funk CK, O'Dell LE, Crawford EF, Koob GF (2006) Corticotropin-releasing factor within the central nucleus of the amygdala mediates enhanced ethanol self-administration in withdrawn, ethanol-dependent rats. J Neurosci 26:11324–11332

    Article  PubMed  CAS  Google Scholar 

  • Funk CK, Zorrilla EP, Lee MJ, Rice KC, Koob GF (2007) Corticotropin-releasing factor 1 antagonists selectively reduce ethanol self-administration in ethanol-dependent rats. Biol Psychiatry 61:78–86

    Article  PubMed  CAS  Google Scholar 

  • Furay AR, Neumaier JF (2011) Opioid receptors: binding that ties. Neuropsychopharmacol 36:2157–2158

    Article  CAS  Google Scholar 

  • Gaffori O, Le Moal M (1979) Disruption of maternal behavior and appearance of cannibalism after ventral mesencephalic tegmentum lesions. Physiol Behav 23:317–323

    Article  PubMed  CAS  Google Scholar 

  • Gainer H, Wray S (1994) Cellular and molecular biology of oxytocin and vasopressin. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven, New York, pp 1099–1129

    Google Scholar 

  • George O, Ghozland S, Azar MR, Cottone P, Zorrilla EP, Parsons LH, O'Dell LE, Richardson HN, Koob GF (2007) CRF-CRF1 system activation mediates withdrawal-induced increases in nicotine self-administration in nicotine-dependent rats. Proc Natl Acad Sci U S A 104:17198–17203

    Article  PubMed  CAS  Google Scholar 

  • Gerfen CR, Young WS 3rd (1988) Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res 460:161–167

    Article  PubMed  CAS  Google Scholar 

  • Gerfen CR, Keefe KA, Gauda EB (1995) D1 and D2 dopamine receptor function in the striatum: coactivation of D1- and D2-dopamine receptors on separate populations of neurons results in potentiated immediate early gene response in D1-containing neurons. J Neurosci 15:8167–8176

    PubMed  CAS  Google Scholar 

  • Gerrits MA, Lesscher HB, van Ree JM (2003) Drug dependence and the endogenous opioid system. Eur Neuropsychopharmacol 13:424–434

    Article  PubMed  CAS  Google Scholar 

  • Getz LL, Hofmann JE (1986) Social organization in free-living prairie voles, Microtus ochrogaster. Behav Ecol Sociobiol 18:275–282

    Article  Google Scholar 

  • Getz LL, Carter CS, Gavish L (1981) The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bonding. Behav Ecol Sociobiol 8:189–194

    Article  Google Scholar 

  • Gillath O, Shaver PR, Baek JM, Chun DS (2008) Genetic correlates of adult attachment style. Pers Soc Psychol Bull 34:1396–1405

    Article  PubMed  Google Scholar 

  • Gingrich B, Liu Y, Cascio C, Wang Z, Insel TR (2000) Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster). Behav Neurosci 114:173–183

    Article  PubMed  CAS  Google Scholar 

  • Goeders NE, Lane JD, Smith JE (1984) Self-administration of methionine enkephalin into the nucleus accumbens. Pharmacol Biochem Behav 20:451–455

    Article  PubMed  CAS  Google Scholar 

  • Goldstein A, Tachibana S, Lowney LI, Hunkapiller M, Hood L (1979) Dynorphin-(1-13), an extraordinarily potent opioid peptide. Proc Natl Acad Sci U S A 76:6666–6670

    Article  PubMed  CAS  Google Scholar 

  • Greenway FL, Fujioka K, Plodkowski RA, Mudaliar S, Guttadauria M, Erickson J, Kim DD, Dunayevich E (2010) Effect of naltrexone plus bupropion on weight loss in overweight and obese adults (COR-I): a multicentre, randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 376:595–605

    Article  PubMed  CAS  Google Scholar 

  • Grieder TE, George O, Tan H, George SR, Le Foll B, Laviolette SR, van der Kooy D (2012) Phasic D1 and tonic D2 dopamine receptor signaling double dissociate the motivational effects of acute nicotine and chronic nicotine withdrawal. Proc Natl Acad Sci U S A 109:3101–3106

    Article  PubMed  CAS  Google Scholar 

  • Grippo AJ, Cushing BS, Carter CS (2007a) Depression-like behavior and stressor-induced neuroendocrine activation in female prairie voles exposed to chronic social isolation. Psychosom Med 69:149–157

    Article  PubMed  Google Scholar 

  • Grippo AJ, Gerena D, Huang J, Kumar N, Shah M, Ughreja R, Carter CS (2007b) Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles. Psychoneuroendocrinol 32:966–980

    Article  CAS  Google Scholar 

  • Guastella AJ, Mitchell PB, Dadds MR (2008) Oxytocin increases gaze to the eye region of human faces. Biol Psychiatry 63:3–5

    Article  PubMed  CAS  Google Scholar 

  • Hansen S, Harthon C, Wallin E, Lofberg L, Svensson K (1991a) The effects of 6-OHDA-induced dopamine depletions in the ventral or dorsal striatum on maternal and sexual behavior in the female rat. Pharmacol Biochem Behav 39:71–77

    Article  PubMed  CAS  Google Scholar 

  • Hansen S, Harthon C, Wallin E, Lofberg L, Svensson K (1991b) Mesotelencephalic dopamine system and reproductive behavior in the female rat: effects of ventral tegmental 6-hydroxydopamine lesions on maternal and sexual responsiveness. Behav Neurosci 105:588–598

    Article  PubMed  CAS  Google Scholar 

  • Hansen S, Bergvall AH, Nyiredi S (1993) Interaction with pups enhances dopamine release in the ventral striatum of maternal rats: a microdialysis study. Pharmacol Biochem Behav 45:673–676

    Article  PubMed  CAS  Google Scholar 

  • Hanson GR, Merchant KM, Letter AA, Bush L, Gibb JW (1988) Characterization of methamphetamine effects on the striatal-nigral dynorphin system. Eur J Pharmacol 155:11–18

    Article  PubMed  CAS  Google Scholar 

  • Heinrichs SC, Koob GF (2004) Corticotropin-releasing factor in brain: a role in activation, arousal, and affect regulation. J Pharmacol Exp Ther 311:427–440

    Article  PubMed  CAS  Google Scholar 

  • Heinrichs SC, Menzaghi F, Pich EM, Baldwin HA, Rassnick S, Britton KT, Koob GF (1994) Anti-stress action of a corticotropin-releasing factor antagonist on behavioral reactivity to stressors of varying type and intensity. Neuropsychopharmacology 11:179–186

    Article  PubMed  CAS  Google Scholar 

  • Henry DJ, White FJ (1995) The persistence of behavioral sensitization to cocaine parallels enhanced inhibition of nucleus accumbens neurons. J Neurosci 15:6287–6299

    PubMed  CAS  Google Scholar 

  • Herman BH, Panksepp J (1978) Effects of morphine and naloxone on separation distress and approach attachment: evidence for opiate mediation of social affect. Pharmacol Biochem Behav 9:213–220

    Article  PubMed  CAS  Google Scholar 

  • Hernandez L, Hoebel BG (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42:1705–1712

    Article  PubMed  CAS  Google Scholar 

  • Hershon HI (1977) Alcohol withdrawal symptoms and drinking behavior. J Stud Alcohol 38:953–971

    PubMed  CAS  Google Scholar 

  • Higham JP, Barr CS, Hoffman CL, Mandalaywala TM, Parker KJ, Maestripieri D (2011) Mu-opioid receptor (OPRM1) variation, oxytocin levels and maternal attachment in free-ranging rhesus macaques Macaca mulatta. Behav Neurosci 125:131–136

    Article  PubMed  CAS  Google Scholar 

  • Hiroi N, White NM (1993) The ventral pallidum area is involved in the acquisition but not expression of the amphetamine conditioned place preference. Neurosci Lett 156:9–12

    Article  PubMed  CAS  Google Scholar 

  • Ho SP, Takahashi LK, Livanov V, Spencer K, Lesher T, Maciag C, Smith MA, Rohrbach KW, Hartig PR, Arneric SP (2001) Attenuation of fear conditioning by antisense inhibition of brain corticotropin releasing factor-2 receptor. Brain Res Mol Brain Res 89:29–40

    Article  PubMed  CAS  Google Scholar 

  • Hoffman DC, Beninger RJ (1988) Selective D1 and D2 dopamine agonists produce opposing effects in place conditioning but not in conditioned taste aversion learning. Pharmacol Biochem Behav 31:1–8

    Article  PubMed  CAS  Google Scholar 

  • Hoffman DC, Dickson PR, Beninger RJ (1988) The dopamine D2 receptor agonists, quinpirole and bromocriptine produce conditioned place preferences. Prog Neuropsychopharmacol Biol Psychiatry 12:315–322

    Article  PubMed  CAS  Google Scholar 

  • Holden C (2001) Compulsive behaviors: "behavioral' addictions: do they exist? Science 294:980–982

    Article  PubMed  CAS  Google Scholar 

  • Horowitz MJ, Siegel B, Holen A, Bonanno GA, Milbrath C, Stinson CH (1997) Diagnostic criteria for complicated grief disorder. Am J Psychiatry 154:904–910

    PubMed  CAS  Google Scholar 

  • Hu XT, White FJ (1997) Dopamine enhances glutamate-induced excitation of rat striatal neurons by cooperative activation of D1 and D2 class receptors. Neurosci Lett 224:61–65

    Article  PubMed  CAS  Google Scholar 

  • Hubner CB, Koob GF (1990) The ventral pallidum plays a role in mediating cocaine and heroin self-administration in the rat. Brain Res 508:20–29

    Article  PubMed  CAS  Google Scholar 

  • Hughes J, Smith TW, Kosterlitz HW, Fothergill LA, Morgan BA, Morris HR (1975) Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature 258:577–580

    Article  PubMed  CAS  Google Scholar 

  • Hurd YL, Brown EE, Finlay JM, Fibiger HC, Gerfen CR (1992) Cocaine self-administration differentially alters mRNA expression of striatal peptides. Brain Res Mol Brain Res 13:165–170

    Article  PubMed  CAS  Google Scholar 

  • Ibragimov R, Kovacs GL, Szabo G, Telegdy G (1987) Microinjection of oxytocin into limbic-mesolimbic brain structures disrupts heroin self-administration behavior—a receptor-mediated event. Life Sci 41:1265–1271

    Article  PubMed  CAS  Google Scholar 

  • Ikemoto S, Panksepp J (1999) The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 31:6–41

    Article  PubMed  CAS  Google Scholar 

  • Insel TR (2003) Is social attachment an addictive disorder? Physiol Behav 79:351–357

    Article  PubMed  CAS  Google Scholar 

  • Insel TR, Shapiro LE (1992) Oxytocin receptor distribution reflects social-organization in monogamous and polygamous voles. Proc Natl Acad Sci U S A 89:5981–5985

    Article  PubMed  CAS  Google Scholar 

  • Insel TR, Wang ZX, Ferris CF (1994) Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J Neurosci 14:5381–5392

    PubMed  CAS  Google Scholar 

  • Insel TR, Preston S, Winslow JT (1995) Mating in the monogamous male: behavioral consequences. Physiol Behav 57:615–627

    Article  PubMed  CAS  Google Scholar 

  • Ismail N, Girard-Beriault F, Nakanishi S, Pfaus JG (2009) Naloxone, but not flupenthixol, disrupts the development of conditioned ejaculatory preference in the male rat. Behav Neurosci 123:992–999

    Article  PubMed  CAS  Google Scholar 

  • Ismayilova N, Shoaib M (2010) Alteration of intravenous nicotine self-administration by opioid receptor agonist and antagonists in rats. Psychopharmacol (Berl) 210:211–220

    Article  CAS  Google Scholar 

  • Isola R, Zhang H, Tejwani GA, Neff NH, Hadjiconstantinou M (2009) Acute nicotine changes dynorphin and prodynorphin mRNA in the striatum. Psychopharmacology (Berl) 201:507–516

    Article  CAS  Google Scholar 

  • Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483–488

    PubMed  CAS  Google Scholar 

  • Kalin NH, Shelton SE, Barksdale CM (1988) Opiate modulation of separation-induced distress in non-human primates. Brain Res 440:285–292

    Article  PubMed  CAS  Google Scholar 

  • Kalin NH, Shelton SE, Lynn DE (1995) Opiate systems in mother and infant primates coordinate intimate contact during reunion. Psychoneuroendocrinol 20:735–742

    Article  CAS  Google Scholar 

  • Karras A, Kane JM (1980) Naloxone reduces cigarette smoking. Life Sci 27:1541–1545

    Article  PubMed  CAS  Google Scholar 

  • Keebaugh AC, Young LJ (2011) Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults. Horm Behav 60:498–504

    Article  PubMed  CAS  Google Scholar 

  • Keer SE, Stern JM (1999) Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol Behav 67:659–669

    Article  PubMed  CAS  Google Scholar 

  • Kelley AE, Berridge KC (2002) The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22:3306–3311

    PubMed  CAS  Google Scholar 

  • Kendrick KM, Keverne EB (1989) 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 Res 505:329–332

    Article  PubMed  CAS  Google Scholar 

  • Kendrick KM, Keverne EB, Baldwin BA (1987) Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology 46:56–61

    Article  PubMed  CAS  Google Scholar 

  • Keverne EB, Kendrick KM (1994) Maternal behaviour in sheep and its neuroendocrine regulation. Acta Paediatr Suppl 397:47–56

    Article  PubMed  CAS  Google Scholar 

  • Khachaturian H, Lewis ME, Schafer MKH, Watson SJ (1985) Anatomy of the CNS opioid systems. Trends Neurosci 8:111–119

    Article  CAS  Google Scholar 

  • Kieffer BL, Befort K, Gaveriaux-Ruff C, Hirth CG (1992) The delta-opioid receptor: isolation of a cDNA by expression cloning and pharmacological characterization. Proc Natl Acad Sci U S A 89:12048–12052

    Article  PubMed  CAS  Google Scholar 

  • Kim SH, Baik SH, Park CS, Kim SJ, Choi SW, Kim SE (2011) Reduced striatal dopamine D2 receptors in people with Internet addiction. NeuroReport 22:407–411

    Article  PubMed  CAS  Google Scholar 

  • Kleiman DG (1977) Monogamy in mammals. Q Rev Biol 52:39–69

    Article  PubMed  CAS  Google Scholar 

  • Knapp RJ, Malatynska E, Collins N, Fang L, Wang JY, Hruby VJ, Roeske WR, Yamamura HI (1995) Molecular biology and pharmacology of cloned opioid receptors. FASEB J 9:516–525

    PubMed  CAS  Google Scholar 

  • Knapp DJ, Overstreet DH, Moy SS, Breese GR (2004) SB242084, flumazenil, and CRA1000 block ethanol withdrawal-induced anxiety in rats. Alcohol 32:101–111

    Article  PubMed  CAS  Google Scholar 

  • Koller G, Zill P, Rujescu D, Ridinger M, Pogarell O, Fehr C, Wodarz N, Bondy B, Soyka M, Preuss UW (2012) Possible association between oprm1 genetic variance at the 118 locus and alcohol dependence in a large treatment sample: relationship to alcohol dependence symptoms. Alcohol Clin Exp Res. doi:10.1111/j.1530-0277.2011.01714.x

  • Koob GF (2008) A role for brain stress systems in addiction. Neuron 59:11–34

    Article  PubMed  CAS  Google Scholar 

  • Koob GF (2010) The role of CRF and CRF-related peptides in the dark side of addiction. Brain Res 1314:3–14

    Article  PubMed  CAS  Google Scholar 

  • Koob GF, Bloom FE (1988) Cellular and molecular mechanisms of drug dependence. Science 242:715–723

    Article  PubMed  CAS  Google Scholar 

  • Koob G, Kreek MJ (2007) Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am J Psychiatry 164:1149–1159

    Article  PubMed  Google Scholar 

  • Koob GF, Zorrilla EP (2010) Neurobiological mechanisms of addiction: focus on corticotropin-releasing factor. Curr Opin Investig Drugs 11:63–71

    PubMed  CAS  Google Scholar 

  • Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E (2005) Oxytocin increases trust in humans. Nature 435:673–676

    Article  PubMed  CAS  Google Scholar 

  • Kovacs GL, Telegdy G (1987) Beta-endorphin tolerance is inhibited by oxytocin. Pharmacol Biochem Behav 26:57–60

    Article  PubMed  CAS  Google Scholar 

  • Kovacs GL, Vanree JM (1985) Behaviorally active oxytocin fragments simultaneously attenuate heroin self-administration and tolerance in rats. Life Sci 37:1895–1900

    Article  PubMed  CAS  Google Scholar 

  • Kovacs GL, Szontagh L, Balaspiri L, Hodi K, Bohus P, Telegdy G (1981) On the mode of action of an oxytocin derivative (Z-Pro-D-Leu) on morphine-dependence in mice. Neuropharmacology 20:647–651

    Article  PubMed  CAS  Google Scholar 

  • Kovacs GL, Faludi M, Falkay G, Telegdy G (1986) Peripheral oxytocin treatment modulates central dopamine transmission in the mouse limbic structures. Neurochem Int 9:481–485

    Article  PubMed  CAS  Google Scholar 

  • Kovacs GL, Sarnyai Z, Izbeki F, Szabo G, Telegdy G, Barth T, Jost K, Brtnik F (1987) Effects of oxytocin-related peptides on acute morphine tolerance: opposite actions by oxytocin and its receptor antagonists. J Pharmacol Exp Ther 241:569–574

    PubMed  CAS  Google Scholar 

  • Kovacs GL, Sarnyai Z, Babarczi E, Szabo G, Telegdy G (1990) The role of oxytocin dopamine interactions in cocaine-induced locomotor hyperactivity. Neuropharmacology 29:365–368

    Article  PubMed  CAS  Google Scholar 

  • Kovacs GL, Sarnyai Z, Szabo G (1998) Oxytocin and addiction: a review. Psychoneuroendocrinology 23:945–962

    Article  PubMed  CAS  Google Scholar 

  • Kreibich AS, Briand L, Cleck JN, Ecke L, Rice KC, Blendy JA (2009) Stress-induced potentiation of cocaine reward: a role for CRF R1 and CREB. Neuropsychopharmacology 34:2609–2617

    Article  PubMed  CAS  Google Scholar 

  • Krivoy WA, Zimmerma E, Lande S (1974) Facilitation of development of resistance to morphine analgesia by desglycinamide9-lysine vasopressin. Proc Natl Acad Sci U S A 71:1852–1856

    Article  PubMed  CAS  Google Scholar 

  • Kroslak T, Laforge KS, Gianotti RJ, Ho A, Nielsen DA, Kreek MJ (2007) The single nucleotide polymorphism A118G alters functional properties of the human mu opioid receptor. J Neurochem 103:77–87

    PubMed  CAS  Google Scholar 

  • Kuzmin AV, Gerrits MA, van Ree JM, Zvartau EE (1997) Naloxone inhibits the reinforcing and motivational aspects of cocaine addiction in mice. Life Sci 60:PL-257–PL-264

    Article  CAS  Google Scholar 

  • LaHoste GJ, Yu J, Marshall JF (1993) Striatal Fos expression is indicative of dopamine D1/D2 synergism and receptor supersensitivity. Proc Natl Acad Sci U S A 90:7451–7455

    Article  PubMed  CAS  Google Scholar 

  • Lakatos K, Toth I, Nemoda Z, Ney K, Sasvari-Szekely M, Gervai J (2000) Dopamine D4 receptor (DRD4) gene polymorphism is associated with attachment disorganization in infants. Mol Psychiatry 5:633–637

    Article  PubMed  CAS  Google Scholar 

  • Le Merrer J, Becker JA, Befort K, Kieffer BL (2009) Reward processing by the opioid system in the brain. Physiol Rev 89:1379–1412

    Article  PubMed  Google Scholar 

  • Lee MR, Gallen CL, Zhang X, Hodgkinson CA, Goldman D, Stein EA, Barr CS (2011) Functional polymorphism of the mu-opioid receptor gene (OPRM1) influences reinforcement learning in humans. PLoS One 6:e24203

    Article  PubMed  CAS  Google Scholar 

  • Leeman RF, Potenza MN (2012) Similarities and differences between pathological gambling and substance use disorders: a focus on impulsivity and compulsivity. Psychopharmacol (Berl) 219:469–490

    Article  CAS  Google Scholar 

  • Light KC, Smith TE, Johns JM, Brownley KA, Hofheimer JA, Amico JA (2000) Oxytocin responsivity in mothers of infants: a preliminary study of relationships with blood pressure during laboratory stress and normal ambulatory activity. Health Psychol 19:560–567

    Article  PubMed  CAS  Google Scholar 

  • Light KC, Grewen KM, Amico JA (2005) More frequent partner hugs and higher oxytocin levels are linked to lower blood pressure and heart rate in premenopausal women. Biol Psychol 69:5–21

    Article  PubMed  Google Scholar 

  • Lim MM, Young LJ (2004) Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience 125:35–45

    Article  PubMed  CAS  Google Scholar 

  • Lim MM, Wang Z, Olazabal DE, Ren X, Terwilliger EF, Young LJ (2004) Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429:754–757

    Article  PubMed  CAS  Google Scholar 

  • Lim MM, Nair HP, Young LJ (2005) Species and sex differences in brain distribution of corticotropin-releasing factor receptor subtypes 1 and 2 in monogamous and promiscuous vole species. J Comp Neurol 487:75–92

    Article  PubMed  CAS  Google Scholar 

  • Lim MM, Tsivkovskaia NO, Bai Y, Young LJ, Ryabinin AE (2006) Distribution of corticotropin-releasing factor and urocortin 1 in the vole brain. Brain Behav Evol 68:229–240

    Article  PubMed  Google Scholar 

  • Lim MM, Liu Y, Ryabinin AE, Bai Y, Wang Z, Young LJ (2007) CRF receptors in the nucleus accumbens modulate partner preference in prairie voles. Horm Behav 51:508–515

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Wang ZX (2003) Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 121:537–544

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Aragona BJ, Young KA, Dietz DM, Kabbaj M, Mazei-Robison M, Nestler EJ, Wang Z (2010) Nucleus accumbens dopamine mediates amphetamine-induced impairment of social bonding in a monogamous rodent species. Proc Natl Acad Sci U S A 107:1217–1222

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Young KA, Curtis JT, Aragona BJ, Wang Z (2011) Social bonding decreases the rewarding properties of amphetamine through a dopamine D1 receptor-mediated mechanism. J Neurosci 31:7960–7966

    Article  PubMed  CAS  Google Scholar 

  • Ljungberg T, Apicella P, Schultz W (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67:145–163

    PubMed  CAS  Google Scholar 

  • Loup F, Tribollet E, Dubois-Dauphin M, Dreifuss JJ (1991) Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res 555:220–232

    Article  PubMed  CAS  Google Scholar 

  • Luijk MP, Roisman GI, Haltigan JD, Tiemeier H, Booth-Laforce C, van Ijzendoorn MH, Belsky J, Uitterlinden AG, Jaddoe VW, Hofman A, Verhulst FC, Tharner A, Bakermans-Kranenburg MJ (2011) Dopaminergic, serotonergic, and oxytonergic candidate genes associated with infant attachment security and disorganization? In search of main and interaction effects. J Child Psychol Psychiatry 52:1295–1307

    Article  PubMed  Google Scholar 

  • Lukas M, Bredewold R, Landgraf R, Neumann ID, Veenema AH (2011) Early life stress impairs social recognition due to a blunted response of vasopressin release within the septum of adult male rats. Psychoneuroendocrinology 36:843–853

    Article  PubMed  CAS  Google Scholar 

  • MacLean PD (1990) The triune brain in evolution: role in paleocerebral functions. Plenum, New York

    Google Scholar 

  • Madison DM (1980) Space use and social structure in meadow voles, Microtus pennsylvanicus. Behav Ecol Sociobiol 7:65–71

    Article  Google Scholar 

  • Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ (1987) Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J Neurosci 7:2445–2464

    PubMed  CAS  Google Scholar 

  • Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ (1988) Anatomy of CNS opioid receptors. Trends Neurosci 11:308–314

    Article  PubMed  CAS  Google Scholar 

  • Mansour A, Fox CA, Meng F, Akil H, Watson SJ (1994a) Kappa 1 receptor mRNA distribution in the rat CNS: comparison to kappa receptor binding and prodynorphin mRNA. Mol Cell Neurosci 5:124–144

    Article  PubMed  CAS  Google Scholar 

  • Mansour A, Fox CA, Thompson RC, Akil H, Watson SJ (1994b) Mu-opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res 643:245–265

    Article  PubMed  CAS  Google Scholar 

  • Martel FL, Nevison CM, Rayment FD, Simpson MJ, Keverne EB (1993) Opioid receptor blockade reduces maternal affect and social grooming in rhesus monkeys. Psychoneuroendocrinology 18:307–321

    Article  PubMed  CAS  Google Scholar 

  • Martel FL, Nevison CM, Simpson MJ, Keverne EB (1995) Effects of opioid receptor blockade on the social behavior of rhesus monkeys living in large family groups. Dev Psychobiol 28:71–84

    Article  PubMed  CAS  Google Scholar 

  • Matthes HW, Maldonado R, Simonin F, Valverde O, Slowe S, Kitchen I, Befort K, Dierich A, Le Meur M, Dolle P, Tzavara E, Hanoune J, Roques BP, Kieffer BL (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383:819–823

    Article  PubMed  CAS  Google Scholar 

  • Mattson BJ, Williams S, Rosenblatt JS, Morrell JI (2001) Comparison of two positive reinforcing stimuli: pups and cocaine throughout the postpartum period. Behav Neurosci 115:683–694

    Article  PubMed  CAS  Google Scholar 

  • McGraw LA, Young LJ (2010) The prairie vole: an emerging model organism for understanding the social brain. Trends Neurosci 33:103–109

    Article  PubMed  CAS  Google Scholar 

  • McGregor IS, Bowen MT (2012) Breaking the loop: oxytocin as a potential treatment for drug addiction. Horm Behav 61:331–339

    Article  PubMed  CAS  Google Scholar 

  • McLaughlin JP, Marton-Popovici M, Chavkin C (2003) Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23:5674–5683

    PubMed  CAS  Google Scholar 

  • Measelle JR, Stice E, Springer DW (2006) A prospective test of the negative affect model of substance abuse: moderating effects of social support. Psychol Addict Behav 20:225–233

    Article  PubMed  Google Scholar 

  • Mehrara BJ, Baum MJ (1990) Naloxone disrupts the expression but not the acquisition by male rats of a conditioned place preference response for an oestrous female. Psychopharmacol (Berl) 101:118–125

    Article  CAS  Google Scholar 

  • Menzaghi F, Howard RL, Heinrichs SC, Vale W, Rivier J, Koob GF (1994) Characterization of a novel and potent corticotropin-releasing factor antagonist in rats. J Pharmacol Exp Ther 269:564–572

    PubMed  CAS  Google Scholar 

  • Merlo Pich E, Lorang M, Yeganeh M, Rodriguez de Fonseca F, Raber J, Koob GF, Weiss F (1995) Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci 15:5439–5447

    PubMed  CAS  Google Scholar 

  • Miczek KA, Fish EW, De Bold JF, De Almeida RM (2002) Social and neural determinants of aggressive behavior: pharmacotherapeutic targets at serotonin, dopamine and gamma-aminobutyric acid systems. Psychopharmacology (Berl) 163:434–458

    Article  CAS  Google Scholar 

  • Miczek KA, Nikulina EM, Shimamoto A, Covington HE 3rd (2011) Escalated or suppressed cocaine reward, tegmental BDNF, and accumbal dopamine caused by episodic versus continuous social stress in rats. J Neurosci 31:9848–9857

    Article  PubMed  CAS  Google Scholar 

  • Miller RL, Baum MJ (1987) Naloxone inhibits mating and conditioned place preference for an estrous female in male rats soon after castration. Pharmacol Biochem Behav 26:781–789

    Article  PubMed  CAS  Google Scholar 

  • Miller NS, Dackis CA, Gold MS (1987) The relationship of addiction, tolerance, and dependence to alcohol and drugs—a neurochemical approach. J Subst Abus Treat 4:197–207

    Article  CAS  Google Scholar 

  • Minozzi S, Amato L, Vecchi S, Davoli M, Kirchmayer U, Verster A (2011) Oral naltrexone maintenance treatment for opioid dependence. Cochrane Database Syst Rev (4):CD001333

  • Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: from structure to function. Physiol Rev 78:189–225

    PubMed  CAS  Google Scholar 

  • Modi ME, Young LJ (2011) D-cycloserine facilitates socially reinforced learning in an animal model relevant to autism spectrum disorders. Biol Psychiatry 70:298–304

    Article  PubMed  CAS  Google Scholar 

  • Mogenson GJ (1987) Limbic-motor integration. In: Epstein AN (ed) Progress in psychobiology and physiological psychology. Academic, New York, pp 117–170

    Google Scholar 

  • Moles A, Kieffer BL, D'Amato FR (2004) Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science 304:1983–1986

    Article  PubMed  CAS  Google Scholar 

  • Nakajima S (1986) Suppression of operant responding in the rat by dopamine D1-receptor blockade with SCH-23390. Physiol Psychol 14:111–114

    CAS  Google Scholar 

  • Nakajima S, Mckenzie GM (1986) Reduction of the rewarding effect of brain-stimulation by a blockade of dopamine D1 receptor with SCH-23390. Pharmacol Biochem Be 24:919–923

    Article  CAS  Google Scholar 

  • Nelson EE, Panksepp J (1998) Brain substrates of infant-mother attachment: contributions of opioids, oxytocin, and norepinephrine. Neurosci Biobehav Rev 22:437–452

    Article  PubMed  CAS  Google Scholar 

  • Nestler EJ, Terwilliger RZ, Walker JR, Sevarino KA, Duman RS (1990) Chronic cocaine treatment decreases levels of the G protein subunits Gi alpha and Go alpha in discrete regions of rat brain. J Neurochem 55:1079–1082

    Article  PubMed  CAS  Google Scholar 

  • Nissen HW (1930) A study of maternal behavior in the white rat by means of the obstruction method. Pegagog Semin J Gen 37:377–393

    Article  Google Scholar 

  • North RA, Williams JT, Surprenant A, Christie MJ (1987) Mu and delta receptors belong to a family of receptors that are coupled to potassium channels. Proc Natl Acad Sci U S A 84:5487–5491

    Article  PubMed  CAS  Google Scholar 

  • Novak G, Seeman P, Le Foll B (2010) Exposure to nicotine produces an increase in dopamine D2(high) receptors: a possible mechanism for dopamine hypersensitivity. Int J Neurosci 120:691–697

    Article  PubMed  CAS  Google Scholar 

  • Numan M (2007) Motivational systems and the neural circuitry of maternal behavior in the rat. Dev Psychobiol 49:12–21

    Article  PubMed  CAS  Google Scholar 

  • Numan M, Insel TR (2003) The neurobiology of parental behavior. Springer, New York

    Google Scholar 

  • Numan M, Numan MJ, Pliakou N, Stolzenberg DS, Mullins OJ, Murphy JM, Smith CD (2005) The effects of D1 or D2 dopamine receptor antagonism in the medial preoptic area, ventral pallidum, or nucleus accumbens on the maternal retrieval response and other aspects of maternal behavior in rats. Behav Neurosci 119:1588–1604

    Article  PubMed  CAS  Google Scholar 

  • Olazabal DE, Young LJ (2006a) Oxytocin receptors in the nucleus accumbens facilitate "spontaneous" maternal behavior in adult female prairie voles. Neuroscience 141:559–568

    Article  PubMed  CAS  Google Scholar 

  • Olazabal DE, Young LJ (2006b) Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Horm Behav 49:681–687

    Article  PubMed  CAS  Google Scholar 

  • Olive MF, Koenig HN, Nannini MA, Hodge CW (2002) Elevated extracellular CRF levels in the bed nucleus of the stria terminalis during ethanol withdrawal and reduction by subsequent ethanol intake. Pharmacol Biochem Behav 72:213–220

    Article  PubMed  CAS  Google Scholar 

  • Olmstead MC, Franklin KB (1997a) The development of a conditioned place preference to morphine: effects of lesions of various CNS sites. Behav Neurosci 111:1313–1323

    Article  PubMed  CAS  Google Scholar 

  • Olmstead MC, Franklin KB (1997b) The development of a conditioned place preference to morphine: effects of microinjections into various CNS sites. Behav Neurosci 111:1324–1334

    Article  PubMed  CAS  Google Scholar 

  • O'Malley SS, Jaffe AJ, Chang G, Schottenfeld RS, Meyer RE, Rounsaville B (1992) Naltrexone and coping skills therapy for alcohol dependence. A controlled study. Arch Gen Psychiatry 49:881–887

    Article  PubMed  Google Scholar 

  • Orians GH (1969) On evolution of mating systems in birds and mammals. Am Nat 103:589

    Article  Google Scholar 

  • Oslin DW, Berrettini W, Kranzler HR, Pettinati H, Gelernter J, Volpicelli JR, O'Brien CP (2003) A functional polymorphism of the mu-opioid receptor gene is associated with naltrexone response in alcohol-dependent patients. Neuropsychopharmacology 28:1546–1552

    Article  PubMed  CAS  Google Scholar 

  • Ott CH (2003) The impact of complicated grief on mental and physical health at various points in the bereavement process. Death Stud 27:249–272

    Article  PubMed  Google Scholar 

  • Panksepp J, Herman B, Conner R, Bishop P, Scott JP (1978) The biology of social attachments: opiates alleviate separation distress. Biol Psychiatry 13:607–618

    PubMed  CAS  Google Scholar 

  • Panksepp J, Najam N, Soares F (1979) Morphine reduces social cohesion in rats. Pharmacol Biochem Behav 11:131–134

    Article  PubMed  CAS  Google Scholar 

  • Panksepp J, Herman BH, Vilberg T, Bishop P, DeEskinazi FG (1980) Endogenous opioids and social behavior. Neurosci Biobehav Rev 4:473–487

    Article  PubMed  CAS  Google Scholar 

  • Panksepp J, Jalowiec J, DeEskinazi FG, Bishop P (1985) Opiates and play dominance in juvenile rats. Behav Neurosci 99:441–453

    Article  PubMed  CAS  Google Scholar 

  • Panksepp J, Nelson E, Siviy S (1994) Brain opioids and mother–infant social motivation. Acta Paediatr Suppl 397:40–46

    Article  PubMed  CAS  Google Scholar 

  • Pecina S, Berridge KC (2000) Opioid site in nucleus accumbens shell mediates eating and hedonic 'liking' for food: map based on microinjection Fos plumes. Brain Res 863:71–86

    Article  PubMed  CAS  Google Scholar 

  • Pecina S, Schulkin J, Berridge KC (2006) Nucleus accumbens corticotropin-releasing factor increases cue-triggered motivation for sucrose reward: paradoxical positive incentive effects in stress? BMC Biol 4:8

    Article  PubMed  CAS  Google Scholar 

  • Pedersen CA, Prange AJ Jr (1979) Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci U S A 76:6661–6665

    Article  PubMed  CAS  Google Scholar 

  • Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA (1994) Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108:1163–1171

    Article  PubMed  CAS  Google Scholar 

  • Peng XQ, Ashby CR Jr, Spiller K, Li X, Li J, Thomasson N, Millan MJ, Mocaer E, Munoz C, Gardner EL, Xi ZX (2009) The preferential dopamine D3 receptor antagonist S33138 inhibits cocaine reward and cocaine-triggered relapse to drug-seeking behavior in rats. Neuropharmacology 56:752–760

    Article  PubMed  CAS  Google Scholar 

  • Perez MF, Ford KA, Goussakov I, Stutzmann GE, Hu XT (2011) Repeated cocaine exposure decreases dopamine D-like receptor modulation of Ca(2+) homeostasis in rat nucleus accumbens neurons. Synapse 65:168–180

    Article  PubMed  CAS  Google Scholar 

  • Pfeiffer A, Brantl V, Herz A, Emrich HM (1986) Psychotomimesis mediated by kappa opiate receptors. Science 233:774–776

    Article  PubMed  CAS  Google Scholar 

  • Plato Rowe CJ (1986) Phaedrus. Aris & Phillips, Warminster, Distributed in the USA and Canada by Humanities Press

    Google Scholar 

  • Pliakas AM, Carlson RR, Neve RL, Konradi C, Nestler EJ, Carlezon WA Jr (2001) Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci 21:7397–7403

    PubMed  CAS  Google Scholar 

  • Pontieri FE, Tanda G, Di Chiara G (1995) Intravenous Cocaine, Morphine, and Amphetamine Preferentially Increase Extracellular Dopamine in the "Shell" as Compared with the "Core" of the Rat Nucleus Accumbens. Proc Natl Acad Sci U S A 92:12304–12308

    Article  PubMed  CAS  Google Scholar 

  • Pontieri FE, Tanda G, Orzi F, Di Chiara G (1996) Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 382:255–257

    Article  PubMed  CAS  Google Scholar 

  • Potenza MN (2006) Should addictive disorders include non-substance-related conditions? Addiction 101:142–151

    Article  PubMed  Google Scholar 

  • Prigerson HG, Maciejewski PK, Reynolds CF 3rd, Bierhals AJ, Newsom JT, Fasiczka A, Frank E, Doman J, Miller M (1995) Inventory of complicated grief: a scale to measure maladaptive symptoms of loss. Psychiatry Res 59:65–79

    Article  PubMed  CAS  Google Scholar 

  • Prigerson HG, Bierhals AJ, Kasl SV, Reynolds CF 3rd, Shear MK, Day N, Beery LC, Newsom JT, Jacobs S (1997) Traumatic grief as a risk factor for mental and physical morbidity. Am J Psychiatry 154:616–623

    PubMed  CAS  Google Scholar 

  • Przewlocka B, Turchan J, Lason W, Przewlocki R (1997) Ethanol withdrawal enhances the prodynorphin system activity in the rat nucleus accumbens. Neurosci Lett 238:13–16

    Article  PubMed  CAS  Google Scholar 

  • Qi J, Yang JY, Wang F, Zhao YN, Song M, Wu CF (2009) Effects of oxytocin on methamphetamine-induced conditioned place preference and the possible role of glutamatergic neurotransmission in the medial prefrontal cortex of mice in reinstatement. Neuropharmacology 56:856–865

    Article  PubMed  CAS  Google Scholar 

  • Resendez SL, Kuhnmuench M, Krzywosinski T, Aragona BJ (2012) Kappa-opioid receptors within the nucleus accumbens shell mediate pair bond maintenance. J Neurosci 32:6771–6784

    Article  PubMed  CAS  Google Scholar 

  • Reynaud M, Karila L, Blecha L, Benyamina A (2010) Is love passion an addictive disorder? Am J Drug Alcohol Ab 36:261–267

    Article  Google Scholar 

  • Richter RM, Weiss F (1999) In vivo CRF release in rat amygdala is increased during cocaine withdrawal in self-administering rats. Synapse 32:254–261

    PubMed  CAS  Google Scholar 

  • Rimondini R, Arlinde C, Sommer W, Heilig M (2002) Long-lasting increase in voluntary ethanol consumption and transcriptional regulation in the rat brain after intermittent exposure to alcohol. FASEB J 16:27–35

    Article  PubMed  CAS  Google Scholar 

  • Robson LE, Gillan MG, Kosterlitz HW (1985) Species differences in the concentrations and distributions of opioid binding sites. Eur J Pharmacol 112:65–71

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Arias M, Minarro J, Aguilar MA, Pinazo J, Simon VM (1998) Effects of risperidone and SCH 23390 on isolation-induced aggression in male mice. Eur Neuropsychopharmacol 8:95–103

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez de Fonseca F, Carrera MR, Navarro M, Koob GF, Weiss F (1997) Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal. Science 276:2050–2054

    Article  PubMed  CAS  Google Scholar 

  • Ross HE, Young LJ (2009) Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrinol 30:534–547

    Article  PubMed  CAS  Google Scholar 

  • Ross HE, Cole CD, Smith Y, Neumann ID, Landgraf R, Murphy AZ, Young LJ (2009a) Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience 162:892–903

    Article  PubMed  CAS  Google Scholar 

  • Ross HE, Freeman SM, Spiegel LL, Ren XH, Terwilliger EF, Young LJ (2009b) Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. J Neurosci 29:1312–1318

    Article  PubMed  CAS  Google Scholar 

  • Rutenberg J (2009) Sanford acknowledges other flirtations. The New York Times, June 30, 2009

  • Sanchis-Segura C, Spanagel R (2006) Behavioural assessment of drug reinforcement and addictive features in rodents: an overview. Addict Biol 11:2–38

    Article  PubMed  Google Scholar 

  • Sanger DJ (1986) Response decrement patterns after neuroleptic and non-neuroleptic drugs. Psychopharmacol (Berl) 89:98–104

    CAS  Google Scholar 

  • Sarnyai Z, Szabo G, Kovacs GL, Telegdy G (1990) Oxytocin attenuates the cocaine-induced exploratory hyperactivity in mice. NeuroReport 1:200–202

    Article  PubMed  CAS  Google Scholar 

  • Sarnyai Z, Babarczy E, Krivan M, Szabo G, Kovacs GL, Barth T, Telegdy G (1991) Selective attenuation of cocaine-induced stereotyped behaviour by oxytocin: putative role of basal forebrain target sites. Neuropeptides 19:51–56

    Article  PubMed  CAS  Google Scholar 

  • Sarnyai Z, Biro E, Babarczy E, Vecsernyes M, Laczi F, Szabo G, Krivan M, Kovacs GL, Telegdy G (1992) Oxytocin modulates behavioural adaptation to repeated treatment with cocaine in rats. Neuropharmacology 31:593–598

    Article  PubMed  CAS  Google Scholar 

  • Sarnyai Z, Biro E, Gardi J, Vecsernyes M, Julesz J, Telegdy G (1995) Brain corticotropin-releasing factor mediates 'anxiety-like' behavior induced by cocaine withdrawal in rats. Brain Res 675:89–97

    Article  PubMed  CAS  Google Scholar 

  • Scavone JL, Asan E, Van Bockstaele EJ (2011) Unraveling glutamate-opioid receptor interactions using high-resolution electron microscopy: implications for addiction-related processes. Exp Neurol 229:207–213

    Article  PubMed  CAS  Google Scholar 

  • Schindler CW, Panlilio LV, Goldberg SR (2002) Second-order schedules of drug self-administration in animals. Psychopharmacology (Berl) 163:327–344

    Article  CAS  Google Scholar 

  • Schneiderman I, Zagoory-Sharon O, Leckman JF, Feldman R (2012) Oxytocin during the initial stages of romantic attachment: relations to couples' interactive reciprocity. Psychoneuroendocrinology 37:1277–1285

    Article  PubMed  CAS  Google Scholar 

  • Seeman P, Tallerico T, Ko F (2004) Alcohol-withdrawn animals have a prolonged increase in dopamine D2high receptors, reversed by general anesthesia: relation to relapse? Synapse 52:77–83

    Article  PubMed  CAS  Google Scholar 

  • Seeman P, McCormick PN, Kapur S (2007) Increased dopamine D2(high) receptors in amphetamine-sensitized rats, measured by the agonist [(3)H](+)Phno. Synapse 61:263–267

    Article  PubMed  CAS  Google Scholar 

  • Self DW, Barnhart WJ, Lehman DA, Nestler EJ (1996) Opposite modulation of cocaine-seeking behavior by D1- and D2-like dopamine receptor agonists. Science 271:1586–1589

    Article  PubMed  CAS  Google Scholar 

  • Shaffer HJ (1999) Strange bedfellows: a critical view of pathological gambling and addiction. Addiction 94:1445–1448

    Article  PubMed  CAS  Google Scholar 

  • Shayit M, Nowak R, Keller M, Weller A (2003) Establishment of a preference by the newborn lamb for its mother: the role of opioids. Behav Neurosci 117:446–454

    Article  PubMed  CAS  Google Scholar 

  • Sheehan TP, Chambers RA, Russell DS (2004) Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Rev 46:71–117

    Article  PubMed  Google Scholar 

  • Shippenberg TS, Bals-Kubik R, Herz A (1987) Motivational properties of opioids: evidence that an activation of delta-receptors mediates reinforcement processes. Brain Res 436:234–239

    Article  PubMed  CAS  Google Scholar 

  • Sibley DR, Monsma FJ Jr, Shen Y (1993) Molecular neurobiology of dopaminergic receptors. Int Rev Neurobiol 35:391–415

    Article  PubMed  CAS  Google Scholar 

  • Siegel A, Roeling TA, Gregg TR, Kruk MR (1999) Neuropharmacology of brain-stimulation-evoked aggression. Neurosci Biobehav Rev 23:359–389

    Article  PubMed  CAS  Google Scholar 

  • Silva MR, Bernardi MM, Felicio LF (2001) Effects of dopamine receptor antagonists on ongoing maternal behavior in rats. Pharmacol Biochem Behav 68:461–468

    Article  PubMed  CAS  Google Scholar 

  • Simonin F, Valverde O, Smadja C, Slowe S, Kitchen I, Dierich A, Le Meur M, Roques BP, Maldonado R, Kieffer BL (1998) Disruption of the kappa-opioid receptor gene in mice enhances sensitivity to chemical visceral pain, impairs pharmacological actions of the selective kappa-agonist U-50,488H and attenuates morphine withdrawal. EMBO J 17:886–897

    Article  PubMed  CAS  Google Scholar 

  • Sinha R, Fuse T, Aubin LR, O'Malley SS (2000) Psychological stress, drug-related cues and cocaine craving. Psychopharmacol (Berl) 152:140–148

    Article  CAS  Google Scholar 

  • Sivam SP (1989) Cocaine selectively increases striatonigral dynorphin levels by a dopaminergic mechanism. J Pharmacol Exp Ther 250:818–824

    PubMed  CAS  Google Scholar 

  • Skelton KH, Gutman DA, Thrivikraman KV, Nemeroff CB, Owens MJ (2007) The CRF1 receptor antagonist R121919 attenuates the neuroendocrine and behavioral effects of precipitated lorazepam withdrawal. Psychopharmacol (Berl) 192:385–396

    Article  CAS  Google Scholar 

  • Skoubis PD, Maidment NT (2003) Blockade of ventral pallidal opioid receptors induces a conditioned place aversion and attenuates acquisition of cocaine place preference in the rat. Neuroscience 119:241–249

    Article  PubMed  CAS  Google Scholar 

  • Smith KS, Berridge KC (2005) The ventral pallidum and hedonic reward: neurochemical maps of sucrose "liking" and food intake. J Neurosci 25:8637–8649

    Article  PubMed  CAS  Google Scholar 

  • Soderman AR, Unterwald EM (2008) Cocaine reward and hyperactivity in the rat: sites of mu opioid receptor modulation. Neuroscience 154:1506–1516

    Article  PubMed  CAS  Google Scholar 

  • Spanagel R, Holter SM (1999) Long-term alcohol self-administration with repeated alcohol deprivation phases: an animal model of alcoholism? Alcohol Alcohol 34:231–243

    PubMed  CAS  Google Scholar 

  • Spanagel R, Herz A, Shippenberg TS (1990) The effects of opioid peptides on dopamine release in the nucleus accumbens: an in vivo microdialysis study. J Neurochem 55:1734–1740

    Article  PubMed  CAS  Google Scholar 

  • Stolzenberg DS, Numan M (2011) Hypothalamic interaction with the mesolimbic DA system in the control of the maternal and sexual behaviors in rats. Neurosci Biobehav Rev 35:826–847

    Article  PubMed  CAS  Google Scholar 

  • Stolzenberg DS, McKenna JB, Keough S, Hancock R, Numan MJ, Numan M (2007) Dopamine D1 receptor stimulation of the nucleus accumbens or the medial preoptic area promotes the onset of maternal behavior in pregnancy-terminated rats. Behav Neurosci 121:907–919

    Article  PubMed  CAS  Google Scholar 

  • Stolzenberg DS, Zhang KY, Luskin K, Ranker L, Bress J, Numan M (2010) Dopamine D(1) receptor activation of adenylyl cyclase, not phospholipase C, in the nucleus accumbens promotes maternal behavior onset in rats. Horm Behav 57:96–104

    Article  PubMed  CAS  Google Scholar 

  • Stout SC, Mortas P, Owens MJ, Nemeroff CB, Moreau J (2000) Increased corticotropin-releasing factor concentrations in the bed nucleus of the stria terminalis of anhedonic rats. Eur J Pharmacol 401:39–46

    Article  PubMed  CAS  Google Scholar 

  • Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321–353

    Article  PubMed  CAS  Google Scholar 

  • Szabo G, Kovacs GL, Telegdy G (1988) Brain monoamines are involved in mediating the action of neurohypophyseal peptide hormones on ethanol tolerance. Acta Physiol Hung 71:459–466

    PubMed  CAS  Google Scholar 

  • Szabo G, Kovacs GL, Telegdy G (1989) Intraventricular administration of neurohypophyseal hormones interferes with the development of tolerance to ethanol. Acta Physiol Hung 73:97–103

    PubMed  CAS  Google Scholar 

  • Tagliaferro P, Morales M (2008) Synapses between corticotropin-releasing factor-containing axon terminals and dopaminergic neurons in the ventral tegmental area are predominantly glutamatergic. J Comp Neurol 506:616–626

    Article  PubMed  CAS  Google Scholar 

  • Takahashi LK, Ho SP, Livanov V, Graciani N, Arneric SP (2001) Antagonism of CRF(2) receptors produces anxiolytic behavior in animal models of anxiety. Brain Res 902:135–142

    Article  PubMed  CAS  Google Scholar 

  • Tamarin RH (ed) (1985) Biology of New World Microtus. Amer Soc Mammal 8:1–893

  • Tanda G, Pontieri FE, Di Chiara G (1997) Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science 276:2048–2050

    Article  PubMed  CAS  Google Scholar 

  • Thomas JA, Birney EC (1979) Parental care and mating system of the prairie vole, Microtus ochrogaster. Behav Ecol Sociobiol 5:171–186

    Article  Google Scholar 

  • Thompson MR, Callaghan PD, Hunt GE, Cornish JL, McGregor IS (2007) A role for oxytocin and 5-HT(1A) receptors in the prosocial effects of 3,4 methylenedioxymethamphetamine ("ecstasy"). Neuroscience 146:509–514

    Article  PubMed  CAS  Google Scholar 

  • Thompson MR, Hunt GE, McGregor IS (2009) Neural correlates of MDMA ("ecstasy")-induced social interaction in rats. Soc Neurosci 4:60–72

    Article  PubMed  CAS  Google Scholar 

  • Tidey JW, Miczek KA (1992a) Effects of SKF 38393 and quinpirole on aggressive, motor and schedule-controlled behaviors in mice. Behav Pharmacol 3:553–565

    Article  PubMed  CAS  Google Scholar 

  • Tidey JW, Miczek KA (1992b) Morphine withdrawal aggression: modification with D1 and D2 receptor agonists. Psychopharmacology (Berl) 108:177–184

    Article  CAS  Google Scholar 

  • Troisi A, Frazzetto G, Carola V, Di Lorenzo G, Coviello M, D'Amato FR, Moles A, Siracusano A, Gross C (2011a) Social hedonic capacity is associated with the A118G polymorphism of the mu-opioid receptor gene (OPRM1) in adult healthy volunteers and psychiatric patients. Soc Neurosci 6:88–97

    Article  PubMed  Google Scholar 

  • Troisi A, Frazzetto G, Carola V, Di Lorenzo G, Coviello M, Siracusano A, Gross C (2011b) Variation in the μ-opioid receptor gene (OPRM1) moderates the influence of early maternal care on fearful attachment. Soc Cogn Affect Neurosci 7:542–547

    Article  PubMed  Google Scholar 

  • Tsunoo A, Yoshii M, Narahashi T (1986) Block of calcium channels by enkephalin and somatostatin in neuroblastoma-glioma hybrid NG108-15 Cells. Proc Natl Acad Sci U S A 83:9832–9836

    Article  PubMed  CAS  Google Scholar 

  • Tucci S, Cheeta S, Seth P, File SE (2003) Corticotropin releasing factor antagonist, alpha-helical CRF(9-41), reverses nicotine-induced conditioned, but not unconditioned, anxiety. Psychopharmacology (Berl) 167:251–256

    CAS  Google Scholar 

  • Turkish S, Cooper SJ (1983) Fluid consumption in water-deprived rats after administration of naloxone or quaternary naloxone. Prog Neuropsychopharmacol Biol Psychiatry 7:835–839

    Article  PubMed  CAS  Google Scholar 

  • Turner RA, Altemus M, Enos T, Cooper B, McGuinness T (1999) Preliminary research on plasma oxytocin in normal cycling women: investigating emotion and interpersonal distress. Psychiatry 62:97–113

    PubMed  CAS  Google Scholar 

  • Ungless MA, Singh V, Crowder TL, Yaka R, Ron D, Bonci A (2003) Corticotropin-releasing factor requires CRF binding protein to potentiate nmda receptors via CRF receptor 2 in dopamine neurons. Neuron 39:401–407

    Article  PubMed  CAS  Google Scholar 

  • Valdez GR, Sabino V, Koob GF (2004) Increased anxiety-like behavior and ethanol self-administration in dependent rats: reversal via corticotropin-releasing factor-2 receptor activation. Alcohol Clin Exp Res 28:865–872

    Article  PubMed  CAS  Google Scholar 

  • van Kesteren RE, Smit AB, Dirks RW, de With ND, Geraerts WP, Joosse J (1992) Evolution of the vasopressin/oxytocin superfamily: characterization of a cDNA encoding a vasopressin-related precursor, preproconopressin, from the mollusc Lymnaea stagnalis. Proc Natl Acad Sci U S A 89:4593–4597

    Article  PubMed  Google Scholar 

  • van Leengoed E, Kerker E, Swanson HH (1987) Inhibition of post-partum maternal behaviour in the rat by injecting an oxytocin antagonist into the cerebral ventricles. J Endocrinol 112:275–282

    Article  PubMed  Google Scholar 

  • Van Ree JM, De Wied D (1977) Effect of neurohypophyseal hormones on morphine-dependence. Psychoneuroendocrinology 2:35–41

    Article  PubMed  Google Scholar 

  • van Ree JM, de Wied D (1980) Involvement of neurohypophyseal peptides in drug-mediated adaptive responses. Pharmacol Biochem Behav 13(Suppl 1):257–263

    PubMed  Google Scholar 

  • van Ree JM, Gerrits MA, Vanderschuren LJ (1999) Opioids, reward and addiction: an encounter of biology, psychology, and medicine. Pharmacol Rev 51:341–396

    PubMed  Google Scholar 

  • Van Ree JM, Niesink RJ, Van Wolfswinkel L, Ramsey NF, Kornet MM, Van Furth WR, Vanderschuren LJ, Gerrits MA, Van den Berg CL (2000) Endogenous opioids and reward. Eur J Pharmacol 405:89–101

    Article  PubMed  Google Scholar 

  • Vanderschuren LJ, Everitt BJ (2004) Drug seeking becomes compulsive after prolonged cocaine self-administration. Science 305:1017–1019

    Article  PubMed  CAS  Google Scholar 

  • Volkow N, Li TK (2005) The neuroscience of addiction. Nat Neurosci 8:1429–1430

    Article  PubMed  CAS  Google Scholar 

  • Volkow ND, Wang GJ, Fowler JS, Gatley SJ, Ding YS, Logan J, Dewey SL, Hitzemann R, Lieberman J (1996a) Relationship between psychostimulant-induced "high" and dopamine transporter occupancy. Proc Natl Acad Sci U S A 93:10388–10392

    Article  PubMed  CAS  Google Scholar 

  • Volkow ND, Wang GJ, Fowler JS, Logan J, Hitzemann R, Ding YS, Pappas N, Shea C, Piscani K (1996b) Decreases in dopamine receptors but not in dopamine transporters in alcoholics. Alcohol Clin Exp Res 20:1594–1598

    Article  PubMed  CAS  Google Scholar 

  • Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Hitzemann R, Chen AD, Dewey SL, Pappas N (1997) Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 386:830–833

    Article  PubMed  CAS  Google Scholar 

  • Volkow ND, Chang L, Wang GJ, Fowler JS, Ding YS, Sedler M, Logan J, Franceschi D, Gatley J, Hitzemann R, Gifford A, Wong C, Pappas N (2001) Low level of brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex. Am J Psychiatry 158:2015–2021

    Article  PubMed  CAS  Google Scholar 

  • Volkow ND, Fowler JS, Wang GJ, Baler R, Telang F (2009) Imaging dopamine's role in drug abuse and addiction. Neuropharmacology 56(Suppl 1):3–8

    Article  PubMed  CAS  Google Scholar 

  • Volkow ND, Wang GJ, Fowler JS, Tomasi D (2012) Addiction circuitry in the human brain. Annu Rev Pharmacol Toxicol 52:321–336

    Article  PubMed  CAS  Google Scholar 

  • Volpicelli JR, Alterman AI, Hayashida M, O'Brien CP (1992) Naltrexone in the treatment of alcohol dependence. Arch Gen Psychiatry 49:876–880

    Article  PubMed  CAS  Google Scholar 

  • Wacker DW, Ludwig M (2012) Vasopressin, oxytocin, and social odor recognition. Horm Behav 61:259–265

    Article  PubMed  CAS  Google Scholar 

  • Walker BM, Koob GF (2008) Pharmacological evidence for a motivational role of kappa-opioid systems in ethanol dependence. Neuropsychopharmacology 33:643–652

    Article  PubMed  CAS  Google Scholar 

  • Walters JR, Bergstrom DA, Carlson JH, Chase TN, Braun AR (1987) D1 dopamine receptor activation required for postsynaptic expression of D2 agonist effects. Science 236:719–722

    Article  PubMed  CAS  Google Scholar 

  • Walum H, Westberg L, Henningsson S, Neiderhiser JM, Reiss D, Igl W, Ganiban JM, Spotts EL, Pedersen NL, Eriksson E, Lichtenstein P (2008) Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc Natl Acad Sci U S A 105:14153–14156

    Article  PubMed  CAS  Google Scholar 

  • Walum H, Lichtenstein P, Neiderhiser JM, Reiss D, Ganiban JM, Spotts EL, Pedersen NL, Anckarsater H, Larsson H, Westberg L (2012) Variation in the oxytocin receptor gene is associated with pair-bonding and social behavior. Biol Psychiatry 71:419–426

    Article  PubMed  CAS  Google Scholar 

  • Wang DV, Tsien JZ (2011) Convergent processing of both positive and negative motivational signals by the VTA dopamine neuronal populations. PLoS One 6:e17047

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Ferris CF, De Vries GJ (1994) Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proc Natl Acad Sci U S A 91:400–404

    Article  PubMed  CAS  Google Scholar 

  • Wang GJ, Volkow ND, Fowler JS, Logan J, Abumrad NN, Hitzemann RJ, Pappas NS, Pascani K (1997a) Dopamine D2 receptor availability in opiate-dependent subjects before and after naloxone-precipitated withdrawal. Neuropsychopharmacology 16:174–182

    Article  PubMed  CAS  Google Scholar 

  • Wang ZX, Hulihan TJ, Insel TR (1997b) Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles. Brain Res 767:321–332

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Yu G, Cascio C, Liu Y, Gingrich B, Insel TR (1999) Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles (Microtus ochrogaster): a mechanism for pair bonding? Behav Neurosci 113:602–611

    Article  PubMed  CAS  Google Scholar 

  • Wang GJ, Volkow ND, Logan J, Pappas NR, Wong CT, Zhu W, Netusil N, Fowler JS (2001) Brain dopamine and obesity. Lancet 357:354–357

    Article  PubMed  CAS  Google Scholar 

  • Wang B, Shaham Y, Zitzman D, Azari S, Wise RA, You ZB (2005) Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin-releasing factor: a role in stress-induced relapse to drug seeking. J Neurosci 25:5389–5396

    Article  PubMed  CAS  Google Scholar 

  • Wang B, You ZB, Rice KC, Wise RA (2007) Stress-induced relapse to cocaine seeking: roles for the CRF(2) receptor and CRF-binding protein in the ventral tegmental area of the rat. Psychopharmacol (Berl) 193:283–294

    Article  CAS  Google Scholar 

  • Warnick JE, McCurdy CR, Sufka KJ (2005) Opioid receptor function in social attachment in young domestic fowl. Behav Brain Res 160:277–285

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • West CH, Schaefer GJ, Michael RP (1983) Increasing the work requirements lowers the threshold of naloxone for reducing self-stimulation in the midbrain of rats. Pharmacol Biochem Behav 18:705–710

    Article  PubMed  CAS  Google Scholar 

  • Wiesner BP, Sheard NM (1933) Maternal behavior in the rat. Oliver & Boyd, Edinburgh

    Google Scholar 

  • Williams JR, Catania KC, Carter CS (1992) Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Horm Behav 26:339–349

    Article  PubMed  CAS  Google Scholar 

  • Wills TA, Cleary SD (1996) How are social support effects mediated? A test with parental support and adolescent substance use. J Personal Soc Psychol 71:937–952

    Article  CAS  Google Scholar 

  • Wilsoncroft WE (1969) Babies by bar-press—maternal behavior in rat. Behav Res Meth Inst 1:229

    Article  Google Scholar 

  • Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR (1993) A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365:545–548

    Article  PubMed  CAS  Google Scholar 

  • Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483–494

    Article  PubMed  CAS  Google Scholar 

  • Wise SP, Murray EA, Gerfen CR (1996) The frontal cortex-basal ganglia system in primates. Crit Rev Neurobiol 10:317–356

    Article  PubMed  CAS  Google Scholar 

  • Wolff K, Tsapakis EM, Winstock AR, Hartley D, Holt D, Forsling ML, Aitchison KJ (2006) Vasopressin and oxytocin secretion in response to the consumption of ecstasy in a clubbing population. J Psychopharmacol 20:400–410

    Article  PubMed  CAS  Google Scholar 

  • Wolffgramm J, Heyne A (1995) From controlled drug intake to loss of control: the irreversible development of drug addiction in the rat. Behav Brain Res 70:77–94

    Article  PubMed  CAS  Google Scholar 

  • Woolverton WL (1986) Effects of a D1 and a D2 dopamine antagonist on the self-administration of cocaine and piribedil by rhesus monkeys. Pharmacol Biochem Behav 24:531–535

    Article  PubMed  CAS  Google Scholar 

  • Woolverton WL, Virus RM (1989) The effects of a D1 and a D2 dopamine antagonist on behavior maintained by cocaine or food. Pharmacol Biochem Behav 32:691–697

    Article  PubMed  CAS  Google Scholar 

  • Woolverton WL, Goldberg LI, Ginos JZ (1984) Intravenous self-administration of dopamine receptor agonists by rhesus monkeys. J Pharmacol Exp Ther 230:678–683

    PubMed  CAS  Google Scholar 

  • Yasuda K, Raynor K, Kong H, Breder CD, Takeda J, Reisine T, Bell GI (1993) Cloning and functional comparison of kappa and delta opioid receptors from mouse brain. Proc Natl Acad Sci U S A 90:6736–6740

    Article  PubMed  CAS  Google Scholar 

  • Yeomans MR, Gray RW (1996) Selective effects of naltrexone on food pleasantness and intake. Physiol Behav 60:439–446

    Article  PubMed  CAS  Google Scholar 

  • Yoshida M, Yokoo H, Mizoguchi K, Kawahara H, Tsuda A, Nishikawa T, Tanaka M (1992) Eating and drinking cause increased dopamine release in the nucleus accumbens and ventral tegmental area in the rat: measurement by in vivo microdialysis. Neurosci Lett 139:73–76

    Article  PubMed  CAS  Google Scholar 

  • Young LJ, Alexander BR (2012) The chemistry between us: love, sex, and the science of attraction. Current, a member of the Penguin Group, New York, NY

  • Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7:1048–1054

    Article  PubMed  CAS  Google Scholar 

  • Young AM, Joseph MH, Gray JA (1992) Increased dopamine release in vivo in nucleus accumbens and caudate nucleus of the rat during drinking: a microdialysis study. Neuroscience 48:871–876

    Article  PubMed  CAS  Google Scholar 

  • Young LJ, Winslow JT, Nilsen R, Insel TR (1997) Species differences in V1a receptor gene expression in monogamous and nonmonogamous voles: behavioral consequences. Behav Neurosci 111:599–605

    Article  PubMed  CAS  Google Scholar 

  • Young LJ, Lim MM, Gingrich B, Insel TR (2001) Cellular mechanisms of social attachment. Horm Behav 40:133–138

    Article  PubMed  CAS  Google Scholar 

  • Young LJ, Murphy Young AZ, Hammock EA (2005) Anatomy and neurochemistry of the pair bond. J Comp Neurol 493:51–57

    Article  PubMed  CAS  Google Scholar 

  • Young KA, Gobrogge KL, Liu Y, Wang Z (2011a) The neurobiology of pair bonding: insights from a socially monogamous rodent. Front Neuroendocrinol 32:53–69

    Article  PubMed  Google Scholar 

  • Young KA, Gobrogge KL, Wang Z (2011b) The role of mesocorticolimbic dopamine in regulating interactions between drugs of abuse and social behavior. Neurosci Biobehav Rev 35:498–515

    Article  PubMed  CAS  Google Scholar 

  • Yudofsky SC, Silver JM, Schneider SE (1987) Pharmacological treatment of aggression. Psychiatr Ann 17:397

    Google Scholar 

  • Zhang Y, Wang D, Johnson AD, Papp AC, Sadee W (2005) Allelic expression imbalance of human mu opioid receptor (OPRM1) caused by variant A118G. J Biol Chem 280:32618–32624

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y, Valdez GR, Fekete EM, Rivier JE, Vale WW, Rice KC, Weiss F, Zorrilla EP (2007) Subtype-selective corticotropin-releasing factor receptor agonists exert contrasting, but not opposite, effects on anxiety-related behavior in rats. J Pharmacol Exp Ther 323:846–854

    Article  PubMed  CAS  Google Scholar 

  • Zorrilla EP, Valdez GR, Weiss F (2001) Changes in levels of regional CRF-like-immunoreactivity and plasma corticosterone during protracted drug withdrawal in dependent rats. Psychopharmacol (Berl) 158:374–381

    Article  CAS  Google Scholar 

  • Zweifel LS, Parker JG, Lobb CJ, Rainwater A, Wall VZ, Fadok JP, Darvas M, Kim MJ, Mizumori SJ, Paladini CA, Phillips PE, Palmiter RD (2009) Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc Natl Acad Sci U S A 106:7281–7288

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

JPB would like to thank his first love for inspiration.

Funding

We acknowledge the funding from MH64692 to LJY, NIH P51OD011132 to YNPRC, and the Emory Scholars Program in Interdisciplinary Neuroscience Research to JPB.

Conflict of interest

The authors declare no conflicts of interest.

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Correspondence to Larry J. Young.

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Burkett, J.P., Young, L.J. The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction. Psychopharmacology 224, 1–26 (2012). https://doi.org/10.1007/s00213-012-2794-x

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  • DOI: https://doi.org/10.1007/s00213-012-2794-x

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