1932

Abstract

Opioid addiction and overdose are at record levels in the United States. This is driven, in part, by their widespread prescription for the treatment of pain, which also increased opportunity for diversion by sensation-seeking users. Despite considerable research on the neurobiology of addiction, treatment options for opioid abuse remain limited. Mood disorders, particularly depression, are often comorbid with both pain disorders and opioid abuse. The endogenous opioid system, a complex neuromodulatory system, sits at the neurobiological convergence point of these three comorbid disease states. We review evidence for dysregulation of the endogenous opioid system as a mechanism for the development of opioid addiction and/or mood disorder. Specifically, individual differences in opioid system function may underlie differences in vulnerability to opioid addiction and mood disorders. We also review novel research, which promises to provide more detailed understanding of individual differences in endogenous opioid neurobiology and its contribution to opioid addiction susceptibility.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-110719-095912
2020-07-08
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/neuro/43/1/annurev-neuro-110719-095912.html?itemId=/content/journals/10.1146/annurev-neuro-110719-095912&mimeType=html&fmt=ahah

Literature Cited

  1. Adler MW, Bendotti C, Ghezzi D, Samanin R, Valzelli L 1975. Dependence to morphine in differentially housed rats. Psychopharmacologia 41:15–18
    [Google Scholar]
  2. Akil H, Gordon J, Hen R, Javitch J, Mayberg H et al. 2018. Treatment resistant depression: a multi-scale, systems biology approach. Neurosci. Biobehav. Rev. 84:272–88
    [Google Scholar]
  3. Akil H, Watson SJ, Young E, Lewis ME, Khachaturian H, Walker JM 1984. Endogenous opioids: biology and function. Annu. Rev. Neurosci. 7:223–55
    [Google Scholar]
  4. Al-Hasani R, Bruchas MR. 2011. Molecular mechanisms of opioid receptor-dependent signaling and behavior. Anesthesiology 115:1363–81
    [Google Scholar]
  5. Al-Hasani R, Wong J-MT, Mabrouk OS, McCall JG, Schmitz GP et al. 2018. In vivo detection of optically-evoked opioid peptide release. eLife 7:e36520
    [Google Scholar]
  6. Am. Soc. Addict. Med 2016. Opioid addiction 2016 facts & figures Fact Sheet, Am. Soc. Addict. Med Chevy Chase, MD:
  7. Ambrosio E, Goldberg SR, Elmer GI 1995. Behavior genetic investigation of the relationship between spontaneous locomotor activity and the acquisition of morphine self-administration behavior. Behav. Pharmacol. 6:229–37
    [Google Scholar]
  8. Amirabadi B, Nikbakht M, Nokani M, Alibeygi N, Safari H 2015. Role of temperament, personality traits and onset age of smoking in predicting opiate dependence. Int. J. High Risk Behav. Addict. 4:e24585
    [Google Scholar]
  9. Bandelow B, Wedekind D. 2015. Possible role of a dysregulation of the endogenous opioid system in antisocial personality disorder. Hum. Psychopharmacol. 30:393–415
    [Google Scholar]
  10. Barwatt JW, Hofford RS, Emery MA, Bates ML, Wellman PJ, Eitan S 2013. Differential effects of methadone and buprenorphine on the response of D2/D3 dopamine receptors in adolescent mice. Drug Alcohol Depend 132:420–26
    [Google Scholar]
  11. Bates ML, Emery MA, Wellman PJ, Eitan S 2014. Social housing conditions influence morphine dependence and the extinction of morphine place preference in adolescent mice. Drug Alcohol Depend 142:283–89
    [Google Scholar]
  12. Bates ML, Emery MA, Wellman PJ, Eitan S 2016. Social environment alters opioid-induced hyperalgesia and antinociceptive tolerance in adolescent mice. Eur. J. Pain 20:998–1009
    [Google Scholar]
  13. Bates MLS, Emery MA, Wellman PJ, Eitan S 2017. Inhibiting social support from massage-like stroking increases morphine dependence. Behav. Pharmacol. 28:642–47
    [Google Scholar]
  14. Bergen SE, Petryshen TL. 2012. Genome-wide association studies of schizophrenia: Does bigger lead to better results?. Curr. Opin. Psychiatry 25:76–82
    [Google Scholar]
  15. Berrettini WH, Alexander R, Ferraro TN, Vogel WH 1994. A study of oral morphine preference in inbred mouse strains. Psychiatr. Genet. 4:81–86
    [Google Scholar]
  16. Bicknell RJ. 1985. Endogenous opioid peptides and hypothalamic neuroendocrine neurones. J. Endocrinol. 107:437–46
    [Google Scholar]
  17. Bond C, LaForge KS, Tian M, Melia D, Zhang S et al. 1998. Single-nucleotide polymorphism in the human mu opioid receptor gene alters β-endorphin binding and activity: possible implications for opiate addiction. PNAS 95:9608–13
    [Google Scholar]
  18. Bozarth MA, Murray A, Wise RA 1989. Influence of housing conditions on the acquisition of intravenous heroin and cocaine self-administration in rats. Pharmacol. Biochem. Behav. 33:903–7
    [Google Scholar]
  19. Bronstein DM, Przewlocki R, Akil H 1990. Effects of morphine treatment on pro-opiomelanocortin systems in rat brain. Brain Res 519:102–11
    [Google Scholar]
  20. Brownstein MJ. 1993. A brief history of opiates, opioid peptides, and opioid receptors. PNAS 90:5391–93
    [Google Scholar]
  21. Bruchas MR, Land BB, Lemos JC, Chavkin C 2010. CRF1-R activation of the dynorphin/kappa opioid system in the mouse basolateral amygdala mediates anxiety-like behavior. PLOS ONE 4:e8528
    [Google Scholar]
  22. Cahill CM, Taylor AM, Cook C, Ong E, Moron JA, Evans CJ 2014. Does the kappa opioid receptor system contribute to pain aversion. ? Front. Pharmacol. 5:253
    [Google Scholar]
  23. Calhoun SE, Meunier CJ, Lee CA, McCarty GS, Sombers LA 2019. Characterization of a multiple-scan-rate voltammetric waveform for real-time detection of met-enkephalin. ACS Chem. Neurosci. 10:2022–32
    [Google Scholar]
  24. Campbell JN. 1996. APS 1995 Presidential address. J. Pain 5:85–88
    [Google Scholar]
  25. Castro DC, Berridge KC. 2014. Opioid hedonic hotspot in nucleus accumbens shell: mu, delta, and kappa maps for enhancement of sweetness “liking” and “wanting. .” J. Neurosci. 34:4239–50
    [Google Scholar]
  26. Cawley NX, Li Z, Loh YP 2016. 60 years of POMC: biosynthesis, trafficking, and secretion of pro-opiomelanocortin-derived peptides. J. Mol. Endocrinol. 56:T77–97
    [Google Scholar]
  27. Chen Y, Chen C, Liu-Chen LY 2007. Dynorphin peptides differentially regulate the human κ opioid receptor. Life Sci 80:1439–48
    [Google Scholar]
  28. Cloninger CR. 1987. A systematic method for clinical description and classification of personality variants. A proposal. Arch. Gen. Psychiatry 44:573–88
    [Google Scholar]
  29. Cole SL, Hofford RS, Evert DJ, Wellman PJ, Eitan S 2013. Social influences on morphine conditioned place preference in adolescent mice. Addict. Biol. 18:274–85
    [Google Scholar]
  30. Compton WM, Jones CM, Baldwin GT 2016. Relationship between nonmedical prescription-opioid use and heroin use. N. Engl. J. Med. 374:154–63
    [Google Scholar]
  31. Coudereau JP, Debray M, Monier C, Bourre JM, Frances H 1996. Effect of isolation on morphine-induced running and changes in body temperature. Prog. Neuropsychopharmacol. Biol. Psychiatry 20:827–38
    [Google Scholar]
  32. Coudereau JP, Debray M, Monier C, Bourre JM, Frances H 1997. Isolation impairs place preference conditioning to morphine but not aversive learning in mice. Psychopharmacology 130:117–23
    [Google Scholar]
  33. de Wit H. 2009. Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict. Biol. 14:22–31
    [Google Scholar]
  34. Deb I, Chakraborty J, Gangopadhyay PK, Choudhury SR, Das S 2010. Single-nucleotide polymorphism (A118G) in exon 1 of OPRM1 gene causes alteration in downstream signaling by mu-opioid receptor and may contribute to the genetic risk for addiction. J. Neurochem. 112:486–96
    [Google Scholar]
  35. Di Cesare Mannelli L, Micheli L, Ghelardini C 2015. Nociceptin/orphanin FQ receptor and pain: feasibility of the fourth opioid family member. Eur. J. Pharmacol. 766:151–54
    [Google Scholar]
  36. Diniz DA, Petrocchi JA, Navarro LC, Souza TC, Castor M et al. 2018. Serotonin induces peripheral antinociception via the opioidergic system. Biomed. Pharmacother. 97:1434–37
    [Google Scholar]
  37. Dreborg S, Sundström G, Larsson TA, Larhammar D 2008. Evolution of vertebrate opioid receptors. PNAS 105:15487–92
    [Google Scholar]
  38. Drolet G, Dumont ÉC, Gosselin I, Kinkead R, Laforest S, Trottier J-F 2001. Role of endogenous opioid system in the regulation of the stress response. Prog. Neuropsychopharmacol. Biol. Psychiatry 25:729–41
    [Google Scholar]
  39. El Rawas R, Thiriet N, Lardeux V, Jaber M, Solinas M 2009. Environmental enrichment decreases the rewarding but not the activating effects of heroin. Psychopharmacology 203:561–70
    [Google Scholar]
  40. Emery MA, Bates ML, Wellman PJ, Eitan S 2015. Differential effects of oxycodone, hydrocodone, and morphine on the responses of D2/D3 dopamine receptors. Behav. Brain Res. 284:37–41
    [Google Scholar]
  41. Emery MA, Bates ML, Wellman PJ, Eitan S 2016. Differential effects of oxycodone, hydrocodone, and morphine on activation levels of signaling molecules. Pain Med 17:908–14
    [Google Scholar]
  42. Emery MA, Bates MLS, Wellman PJ, Eitan S 2017a. Hydrocodone, but neither morphine nor oxycodone, is effective in suppressing burn-induced mechanical allodynia in the uninjured foot contralateral to the burn. J. Burn Care Res. 38:319–26
    [Google Scholar]
  43. Emery MA, Bates MLS, Wellman PJ, Eitan S 2017b. Hydrocodone is more effective than morphine or oxycodone in suppressing the development of burn-induced mechanical allodynia. Pain Med 18:2170–80
    [Google Scholar]
  44. Emery MA, Eitan S. 2019. Members of the same pharmacological family are not alike: different opioids, different consequences, hope for the opioid crisis. ? Prog. Neuropsychopharmacol. Biol. Psychiatry 92:428–49
    [Google Scholar]
  45. Flagel SB, Chaudhury S, Waselus M, Kelly R, Sewani S et al. 2016. Genetic background and epigenetic modifications in the core of the nucleus accumbens predict addiction-like behavior in a rat model. PNAS 113:E2861–70
    [Google Scholar]
  46. Ford JA, Pomykacz C, Szalewski A, Esteban McCabe S, Schepis TS 2020. Friends and relatives as sources of prescription opioids for misuse among young adults: the significance of physician source and race/ethnic differences. Subst. Abus. 41:93–100
    [Google Scholar]
  47. Galaj E, Manuszak M, Ranaldi R 2016. Environmental enrichment as a potential intervention for heroin seeking. Drug Alcohol Depend 163:195–201
    [Google Scholar]
  48. Ganapathy V, Miyauchi S. 2005. Transport systems for opioid peptides in mammalian tissues. AAPS J 7:E852–56
    [Google Scholar]
  49. Gassaway MM, Rives ML, Kruegel AC, Javitch JA, Sames D 2014. The atypical antidepressant and neurorestorative agent tianeptine is a μ-opioid receptor agonist. Transl. Psychiatry 4:e411
    [Google Scholar]
  50. Goesling J, Henry MJ, Moser SE, Rastogi M, Hassett AL et al. 2015. Symptoms of depression are associated with opioid use regardless of pain severity and physical functioning among treatment-seeking patients with chronic pain. J. Pain 16:844–51
    [Google Scholar]
  51. Gutstein HB, Akil H. 2005. Opioid analgesics. Goodman & Gilman's The Pharmacological Basis of Therapeutics LL Brunton, JS Lazo, K Parker 547–90 New York: McGraw-Hill
    [Google Scholar]
  52. Hall FS, Drgonova J, Jain S, Uhl GR 2013. Implications of genome wide association studies for addiction: Are our a priori assumptions all wrong?. Pharmacol. Ther. 140:267–79
    [Google Scholar]
  53. Hedegaard H, Minino AM, Warner M 2018. Drug overdose deaths in the United States, 1999–2017 NCHS Data Brief 329, Natl. Cent. Health Stat Hyattsville, MD:
  54. Hodgson SR, Hofford RS, Roberts KW, Wellman PJ, Eitan S 2010. Socially induced morphine pseudosensitization in adolescent mice. Behav. Pharmacol. 21:112–20
    [Google Scholar]
  55. Hofford RS, Chow JJ, Beckmann JS, Bardo MT 2017. Effects of environmental enrichment on self-administration of the short-acting opioid remifentanil in male rats. Psychopharmacology 234:3499–506
    [Google Scholar]
  56. Ikeda K, Ide S, Han W, Hayashida M, Uhl GR, Sora I 2005. How individual sensitivity to opiates can be predicted by gene analyses. Trends Pharmacol. Sci. 26:311–17
    [Google Scholar]
  57. Inagaki TK. 2018. Opioids and social connection. Curr. Dir. Psychol. Sci. 27:85–90
    [Google Scholar]
  58. Inciardi JA. 1986. The War on Drugs: Heroin, Cocaine, Crime, and Public Policy Palo Alto, CA: Mayfield Publishing
  59. Inui T, Shimura T. 2017. Activation of mu-opioid receptors in the ventral pallidum decreases the negative hedonic evaluation of a conditioned aversive taste in rats. Behav. Brain Res. 320:391–99
    [Google Scholar]
  60. Jassar H, Nascimento TD, Kaciroti N, DosSantos MF, Danciu T et al. 2019. Impact of chronic migraine attacks and their severity on the endogenous μ-opioid neurotransmission in the limbic system. NeuroImage Clin 23:101905
    [Google Scholar]
  61. Jones MR, Viswanath O, Peck J, Kaye AD, Gill JS, Simopoulos TT 2018. A brief history of the opioid epidemic and strategies for pain medicine. Pain Ther 7:13–21
    [Google Scholar]
  62. Kathmann M, Flau K, Redmer A, Trankle C, Schlicker E 2006. Cannabidiol is an allosteric modulator at mu- and delta-opioid receptors. Naunyn-Schmiedeberg's Arch. Pharmacol. 372:354–61
    [Google Scholar]
  63. Kendler KS, Jacobson KC, Prescott CA, Neale MC 2003. Specificity of genetic and environmental risk factors for use and abuse/dependence of cannabis, cocaine, hallucinogens, sedatives, stimulants, and opiates in male twins. Am. J. Psychiatry 160:687–95
    [Google Scholar]
  64. Kennedy BC, Panksepp JB, Runckel PA, Lahvis GP 2012. Social influences on morphine-conditioned place preference in adolescent BALB/cJ and C57BL/6J mice. Psychopharmacology 219:923–32
    [Google Scholar]
  65. Kennedy SE, Koeppe RA, Young EA, Zubieta JK 2006. Dysregulation of endogenous opioid emotion regulation circuitry in major depression in women. Arch. Gen. Psychiatry 63:1199–208
    [Google Scholar]
  66. Khan AA, Jacobson KC, Gardner CO, Prescott CA, Kendler KS 2005. Personality and comorbidity of common psychiatric disorders. Br. J. Psychiatry 186:190–96
    [Google Scholar]
  67. Kiguchi N, Ding H, Ko MC 2016. Central N/OFQ-NOP receptor system in pain modulation. Adv. Pharmacol. 75:217–43
    [Google Scholar]
  68. Koepp MJ, Hammers A, Lawrence AD, Asselin MC, Grasby PM, Bench CJ 2009. Evidence for endogenous opioid release in the amygdala during positive emotion. Neuroimage 44:252–56
    [Google Scholar]
  69. Koob GF. 2015. The dark side of emotion: the addiction perspective. Eur. J. Pharmacol. 753:73–87
    [Google Scholar]
  70. Liu SS, Pickens S, Burma NE, Ibarra-Lecue I, Yang H et al. 2019. Kappa opioid receptors drive a tonic aversive component of chronic pain. J. Neurosci. 39:4162–78
    [Google Scholar]
  71. Liu Y, Blackwood DH, Caesar S, de Geus EJC, Farmer A et al. 2011. Meta-analysis of genome-wide association data of bipolar disorder and major depressive disorder. Mol. Psychiatry 16:2–4
    [Google Scholar]
  72. Livingston KE, Traynor JR. 2018. Allostery at opioid receptors: modulation with small molecule ligands. Br. J. Pharmacol. 175:2846–56
    [Google Scholar]
  73. Llorca-Torralba M, Pilar-Cuellar F, Bravo L, Bruzos-Cidon C, Torrecilla M et al. 2019. Opioid activity in the locus coeruleus is modulated by chronic neuropathic pain. Mol. Neurobiol. 56:4135–50
    [Google Scholar]
  74. Lutz PE, Gross JA, Dhir SK, Maussion G, Yang J et al. 2018. Epigenetic regulation of the kappa opioid receptor by child abuse. Biol. Psychiatry 84:751–61
    [Google Scholar]
  75. Lutz PE, Kieffer BL. 2013. Opioid receptors: distinct roles in mood disorders. Trends Neurosci 36:195–206
    [Google Scholar]
  76. Mague SD, Isiegas C, Huang P, Liu-Chen LY, Lerman C, Blendy JA 2009. Mouse model of OPRM1 (A118G) polymorphism has sex-specific effects on drug-mediated behavior. PNAS 106:10847–52
    [Google Scholar]
  77. Manchikanti L, Giordano J, Boswell MV, Fellows B, Manchukonda R, Pampati V 2007. Psychological factors as predictors of opioid abuse and illicit drug use in chronic pain patients. J. Opioid Manag. 3:89–100
    [Google Scholar]
  78. Mansour A, Hoversten MT, Taylor LP, Watson SJ, Akil H 1995. The cloned μ, δ and κ receptors and their endogenous ligands: evidence for two opioid peptide recognition cores. Brain Res 700:89–98
    [Google Scholar]
  79. Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ 1988. Anatomy of CNS opioid receptors. Trends Neurosci 11:308–14
    [Google Scholar]
  80. Margolis EB, Fujita W, Devi LA, Fields HL 2017. Two delta opioid receptor subtypes are functional in single ventral tegmental area neurons, and can interact with the mu opioid receptor. Neuropharmacology 123:420–32
    [Google Scholar]
  81. Marinova Z, Vukojević V, Surcheva S, Yakovleva T, Cebers G et al. 2005. Translocation of dynorphin neuropeptides across the plasma membrane: a putative mechanism of signal transmission. J. Biol. Chem. 280:26360–70
    [Google Scholar]
  82. Massaly N, Copits BA, Wilson-Poe AR, Hipolito L, Markovic T et al. 2019. Pain-induced negative affect is mediated via recruitment of the nucleus accumbens kappa opioid system. Neuron 102:564–73.e6
    [Google Scholar]
  83. Max MB. 1990. Improving outcomes of analgesic treatment: Is education enough. ? Ann. Intern. Med. 113:885–89
    [Google Scholar]
  84. Meguro Y, Miyano K, Hirayama S, Yoshida Y, Ishibashi N et al. 2018. Neuropeptide oxytocin enhances μ opioid receptor signaling as a positive allosteric modulator. J. Pharmacol. Sci. 137:67–75
    [Google Scholar]
  85. Merikangas KR, Stolar M, Stevens DE, Goulet J, Preisig MA et al. 1998. Familial transmission of substance use disorders. Arch. Gen. Psychiatry 55:973–79
    [Google Scholar]
  86. Merlin MD. 2003. Archaeological evidence for the tradition of psychoactive plant use in the Old World. Econ. Bot. 57:295–323
    [Google Scholar]
  87. Meunier JC, Mollereau C, Toll L, Suaudeau C, Moisand C et al. 1995. Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 377:532–35
    [Google Scholar]
  88. Miech R, Johnston L, O'Malley PM, Keyes KM, Heard K 2015. Prescription opioids in adolescence and future opioid misuse. Pediatrics 136:e1169–77
    [Google Scholar]
  89. Milivojevic D, Milovanovic SD, Jovanovic M, Svrakic DM, Svrakic NM et al. 2012. Temperament and character modify risk of drug addiction and influence choice of drugs. Am. J. Addict. 21:462–67
    [Google Scholar]
  90. Mollereau C, Parmentier M, Mailleux P, Butour JL, Moisand C et al. 1994. ORL1, a novel member of the opioid receptor family: cloning, functional expression and localization. FEBS Lett 341:33–38
    [Google Scholar]
  91. Mongi-Bragato B, Avalos MP, Guzman AS, Bollati FA, Cancela LM 2018. Enkephalin as a pivotal player in neuroadaptations related to psychostimulant addiction. Front. Psychiatry 9:222
    [Google Scholar]
  92. Morgan JP. 1985. American opiophobia: customary underutilization of opioid analgesics. Adv. Alcohol Subst. Abuse 5:163–73
    [Google Scholar]
  93. Murphy NP, Lam HA, Maidment NT 2001. A comparison of morphine-induced locomotor activity and mesolimbic dopamine release in C57BL6, 129Sv and DBA2 mice. J. Neurochem. 79:626–35
    [Google Scholar]
  94. Panksepp J, Nelson E, Siviy S 1994. Brain opioids and mother-infant social motivation. Acta Paediatr. Suppl. 397:40–46
    [Google Scholar]
  95. Parker KE, Pedersen CE, Gomez AM, Spangler SM, Walicki MC et al. 2019. A paranigral VTA nociceptin circuit that constrains motivation for reward. Cell 178:653–71.e19
    [Google Scholar]
  96. Pasternak GW. 2004. Multiple opiate receptors: déjà vu all over again. Neuropharmacology 47:312–23
    [Google Scholar]
  97. Pasternak GW, Pan Y-X. 2013. Mu opioids and their receptors: evolution of a concept. Pharmacol. Rev. 65:1257–317
    [Google Scholar]
  98. Pecina M, Karp JF, Mathew S, Todtenkopf MS, Ehrich EW, Zubieta JK 2019. Endogenous opioid system dysregulation in depression: implications for new therapeutic approaches. Mol. Psychiatry 24:576–87
    [Google Scholar]
  99. Pecina S, Berridge KC. 2005. Hedonic hot spot in nucleus accumbens shell: Where do μ-opioids cause increased hedonic impact of sweetness. ? J. Neurosci. 25:11777–86
    [Google Scholar]
  100. Peck JA, Galaj E, Eshak S, Newman KL, Ranaldi R 2015. Environmental enrichment induces early heroin abstinence in an animal conflict model. Pharmacol. Biochem. Behav. 138:20–25
    [Google Scholar]
  101. Pfeiffer A, Herz A. 1984. Endocrine actions of opioids. Horm. Metab. Res. 16:386–97
    [Google Scholar]
  102. Piltonen M, Parisien M, Grégoire S, Chabot-Doré A-J, Jafarnejad SM et al. 2019. Alternative splicing of the delta-opioid receptor gene suggests existence of new functional isoforms. Mol. Neurobiol. 56:2855–69
    [Google Scholar]
  103. Porter J, Jick H. 1980. Addiction rare in patients treated with narcotics. N. Engl. J. Med. 302:123
    [Google Scholar]
  104. Pradhan AA, Smith ML, Kieffer BL, Evans CJ 2012. Ligand-directed signalling within the opioid receptor family. Br. J. Pharmacol. 167:960–69
    [Google Scholar]
  105. Prater KE, Aurbach EL, Larcinese HK, Smith TN, Turner CA et al. 2017. Selectively bred rats provide a unique model of vulnerability to PTSD-like behavior and respond differentially to FGF2 augmentation early in life. Neuropsychopharmacology 42:1706–14
    [Google Scholar]
  106. Prossin AR, Love TM, Koeppe RA, Zubieta JK, Silk KR 2010. Dysregulation of regional endogenous opioid function in borderline personality disorder. Am. J. Psychiatry 167:925–33
    [Google Scholar]
  107. Ragen BJ, Maninger N, Mendoza SP, Bales KL 2015. The effects of morphine, naloxone, and κ opioid manipulation on endocrine functioning and social behavior in monogamous titi monkeys (Callicebus cupreus). Neuroscience 287:32–42
    [Google Scholar]
  108. Reed B, Butelman ER, Yuferov V, Randesi M, Kreek MJ 2014. Genetics of opiate addiction. Curr. Psychiatry Rep. 16:504
    [Google Scholar]
  109. Resendez SL, Keyes PC, Day JJ, Hambro C, Austin CJ et al. 2016. Dopamine and opioid systems interact within the nucleus accumbens to maintain monogamous pair bonds. eLife 5:e15325
    [Google Scholar]
  110. Ribeiro SC, Kennedy SE, Smith YR, Stohler CS, Zubieta JK 2005. Interface of physical and emotional stress regulation through the endogenous opioid system and μ-opioid receptors. Prog. Neuropsychopharmacol. Biol. Psychiatry 29:1264–80
    [Google Scholar]
  111. Robledo P, Berrendero F, Ozaita A, Maldonado R 2008. Advances in the field of cannabinoid–opioid cross-talk. Addict. Biol. 13:213–24
    [Google Scholar]
  112. Rosenthal SM. 2009. Social pain and opioid use. CMAJ 181:827
    [Google Scholar]
  113. Rubin BS, Bridges RS. 1984. Disruption of ongoing maternal responsiveness in rats by central administration of morphine sulfate. Brain Res 307:91–97
    [Google Scholar]
  114. Samuels BA, Nautiyal KM, Kruegel AC, Levinstein MR, Magalong VM et al. 2017. The behavioral effects of the antidepressant tianeptine require the mu-opioid receptor. Neuropsychopharmacology 42:2052–63
    [Google Scholar]
  115. Scherrer JF, Svrakic DM, Freedland KE, Chrusciel T, Balasubramanian S et al. 2014. Prescription opioid analgesics increase the risk of depression. J. Gen. Intern. Med. 29:491–99
    [Google Scholar]
  116. Schiff PL Jr 2002. Opium and its alkaloids. Am. J. Pharm. Educ. 66:186–94
    [Google Scholar]
  117. Schmitz R. 1985. Friedrich Wilhelm Serturner and the discovery of morphine. Pharm. Hist. 27:61–74
    [Google Scholar]
  118. Sharp BM, Chen H. 2019. Neurogenetic determinants and mechanisms of addiction to nicotine and smoked tobacco. Eur. J. Neurosci. 50:2164–79
    [Google Scholar]
  119. Sher L. 1998. The role of the endogenous opioid system in the pathogenesis of anxiety disorders. Med. Hypotheses 50:473–74
    [Google Scholar]
  120. Shibasaki M, Watanabe K, Takeda K, Itoh T, Tsuyuki T et al. 2013. Effect of chronic ethanol treatment on μ-opioid receptor function, interacting proteins and morphine-induced place preference. Psychopharmacology 228:207–15
    [Google Scholar]
  121. Shoaib M, Spanagel R, Stohr T, Shippenberg TS 1995. Strain differences in the rewarding and dopamine-releasing effects of morphine in rats. Psychopharmacology 117:240–47
    [Google Scholar]
  122. Stead JDH, Clinton S, Neal C, Schneider J, Jama A et al. 2006. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet. 36:697–712
    [Google Scholar]
  123. Stedenfeld KA, Clinton SM, Kerman IA, Akil H, Watson SJ, Sved AF 2011. Novelty-seeking behavior predicts vulnerability in a rodent model of depression. Physiol. Behav. 103:210–16
    [Google Scholar]
  124. Stoeber M, Jullié D, Lobingier BT, Laeremans T, Steyaert J et al. 2018. A genetically encoded biosensor reveals location bias of opioid drug action. Neuron 98:963–76.e5
    [Google Scholar]
  125. Tao R, Auerbach SB. 2005. μ-Opioids disinhibit and κ-opioids inhibit serotonin efflux in the dorsal raphe nucleus. Brain Res 1049:70–79
    [Google Scholar]
  126. Tejeda HA, Bonci A. 2019. Dynorphin/kappa-opioid receptor control of dopamine dynamics: implications for negative affective states and psychiatric disorders. Brain Res 1713:91–101
    [Google Scholar]
  127. Terracciano A, Löckenhoff CE, Crum RM, Bienvenu OJ, Costa PT Jr 2008. Five-Factor Model personality profiles of drug users. BMC Psychiatry 8:22
    [Google Scholar]
  128. Torres-Berrio A, Nava-Mesa MO. 2019. The opioid system in stress-induced memory disorders: from basic mechanisms to clinical implications in post-traumatic stress disorder and Alzheimer's disease. Prog. Neuropsychopharmacol. Biol. Psychiatry 88:327–38
    [Google Scholar]
  129. Trujillo KA, Akil H. 1991. Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 251:85–87
    [Google Scholar]
  130. Trujillo KA, Akil H. 1994. Inhibition of opiate tolerance by non-competitive N-methyl-d-aspartate receptor antagonists. Brain Res 633:178–88
    [Google Scholar]
  131. Trujillo KA, Bronstein DM, Sanchez IO, Akil H 1995. Effects of chronic opiate and opioid antagonist treatment on striatal opioid peptides. Brain Res 698:69–78
    [Google Scholar]
  132. Tsuang MT, Bar JL, Harley RM, Lyons MJ 2001. The Harvard Twin Study of Substance Abuse: what we have learned. Harv. Rev. Psychiatry 9:267–79
    [Google Scholar]
  133. Tsuang MT, Lyons MJ, Meyer JM, Doyle T, Eisen SA et al. 1998. Co-occurrence of abuse of different drugs in men: the role of drug-specific and shared vulnerabilities. Arch. Gen. Psychiatry 55:967–72
    [Google Scholar]
  134. Turchan J, Maj M, Przewlocka B, Przewlocki R 2002. Effect of cocaine and amphetamine on biosynthesis of proenkephalin and prodynorphin in some regions of the rat limbic system. Pol. J. Pharmacol. 54:367–72
    [Google Scholar]
  135. Turchan J, Przewlocka B, Lason W, Przewlocki R 1998. Effects of repeated psychostimulant administration on the prodynorphin system activity and kappa opioid receptor density in the rat brain. Neuroscience 85:1051–59
    [Google Scholar]
  136. Turner CA, Hagenauer MH, Aurbach EL, Maras PM, Fournier CL et al. 2019. Effects of early-life FGF2 on ultrasonic vocalizations (USVs) and the mu-opioid receptor in male Sprague-Dawley rats selectively-bred for differences in their response to novelty. Brain Res 1715:106–14
    [Google Scholar]
  137. US Natl. Acad. Sci. Eng. Med 2019. Medications for opioid use disorder save lives Rep., US Natl. Acad. Sci. Eng. Med Washington, DC:
  138. Van den Berg CL, Kitchen I, Gerrits MA, Spruijt BM, Van Ree JM 1999. Morphine treatment during juvenile isolation increases social activity and opioid peptides release in the adult rat. Brain Res 830:16–23
    [Google Scholar]
  139. Van Zee A. 2009. The promotion and marketing of OxyContin: commercial triumph, public health tragedy. Am. J. Public Health 99:221–27
    [Google Scholar]
  140. Venniro M, Zhang M, Shaham Y, Caprioli D 2016. Incubation of methamphetamine but not heroin craving after voluntary abstinence in male and female rats. Neuropsychopharmacology 42:1126–35
    [Google Scholar]
  141. Verhulst B, Neale MC, Kendler KS 2015. The heritability of alcohol use disorders: a meta-analysis of twin and adoption studies. Psychol. Med. 45:1061–72
    [Google Scholar]
  142. Vowles KE, McEntee ML, Julnes PS, Frohe T, Ney JP, van der Goes DN 2015. Rates of opioid misuse, abuse, and addiction in chronic pain: a systematic review and data synthesis. Pain 156:569–76
    [Google Scholar]
  143. Wang A-L, Lowen SB, Elman I, Shi Z, Fairchild VP et al. 2018. Sustained opioid antagonism modulates striatal sensitivity to baby schema in opioid use disorder. J. Subst. Abuse Treat. 85:70–77
    [Google Scholar]
  144. Watson SJ, Akil H, Fischli W, Goldstein A, Zimmerman E et al. 1982. Dynorphin and vasopressin: common localization in magnocellular neurons. Science 216:85–87
    [Google Scholar]
  145. Wei L-N, Hu X, Bi J, Loh H 2000. Post-transcriptional regulation of mouse κ-opioid receptor expression. Mol. Pharmacol. 57:401–8
    [Google Scholar]
  146. Williams NR, Heifets BD, Blasey C, Sudheimer K, Pannu J et al. 2018. Attenuation of antidepressant effects of ketamine by opioid receptor antagonism. Am. J. Psychiatry 175:1205–15
    [Google Scholar]
  147. Young EA, Lewis J, Akil H 1986. The preferential release of beta-endorphin from the anterior pituitary lobe by corticotropin releasing factor (CRF). Peptides 7:603–7
    [Google Scholar]
  148. Zarate CA Jr, Singh JB, Carlson PJ, Brutsche NE, Ameli R et al. 2006. A randomized trial of an N-methyl-d-aspartate antagonist in treatment-resistant major depression. Arch. Gen. Psychiatry 63:856–64
    [Google Scholar]
  149. Zhang Y, Picetti R, Butelman ER, Ho A, Blendy JA, Kreek MJ 2015. Mouse model of the OPRM1 (A118G) polymorphism: differential heroin self-administration behavior compared with wild-type mice. Neuropsychopharmacology 40:1091–100
    [Google Scholar]
  150. Zhou Z, Blandino P, Yuan Q, Shen P-H, Hodgkinson CA et al. 2019. Exploratory locomotion, a predictor of addiction vulnerability, is oligogenic in rats selected for this phenotype. PNAS 116:13107–15
    [Google Scholar]
  151. Zuckerman M, Kuhlman DM. 2000. Personality and risk-taking: common biosocial factors. J. Pers. 68:999–1029
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-110719-095912
Loading
/content/journals/10.1146/annurev-neuro-110719-095912
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error