Psychopharmacology

, Volume 218, Issue 1, pp 257–269 | Cite as

Prevention of social stress-escalated cocaine self-administration by CRF-R1 antagonist in the rat VTA

  • Christopher O. Boyson
  • Tarciso T. Miguel
  • Isabel M. Quadros
  • Joseph F. DeBold
  • Klaus A. Miczek
Original Investigation

Abstract

Rationale

Intermittent exposure to social defeat stress can induce long-term neural plasticity that may influence escalated cocaine-taking behavior. Stressful encounters can lead to activation of dopamine neurons in the ventral tegmental area (VTA), which are modulated by corticotropin releasing factor (CRF) neurons.

Objective

The study aims to prevent the effects of intermittently scheduled, brief social defeat stress on subsequent intravenous (IV) cocaine self-administration by pretreatment with a CRF receptor subtype 1 (CRF-R1) antagonist.

Materials and methods

Long–Evans rats were submitted to four intermittent social defeat experiences separated by 72 h over 10 days. Two experiments examined systemic or intra-VTA antagonism of CRF-R1 subtype during stress on the later expression of locomotor sensitization and cocaine self-administration during fixed (0.75 mg/kg/infusion) and progressive ratio schedules of reinforcement (0.3 mg/kg/infusion), including a continuous 24-h “binge” (0.3 mg/kg/infusion).

Results

Pretreatment with a CRF-R1 antagonist, CP 154,526, (20 mg/kg i.p.) prior to each social defeat episode prevented the development of stress-induced locomotor sensitization to a cocaine challenge and prevented escalated cocaine self-administration during a 24-h “binge”. In addition, pretreatment with a CRF-R1 antagonist (0.3 μg/0.5 μl/side) into the VTA prior to each social defeat episode prevented stress-induced locomotor sensitization to a cocaine challenge and prevented escalated cocaine self-administration during a 24-h “binge”.

Conclusions

The current results suggest that CRF-R1 subtype in the VTA is critically involved in the development of stress-induced locomotor sensitization which may contribute to escalated cocaine self-administration during continuous access in a 24-h “binge”.

Keywords

Stress Locomotor sensitization Escalated cocaine self-administration CRF-R1 CP 154,526 VTA 

References

  1. Abercrombie ED, Keefe KA, DiFrischia DS, Zigmond MJ (1989) Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 52:1655–1658PubMedCrossRefGoogle Scholar
  2. Bhatnagar S, Vining C (2003) Facilitation of hypothalamic–pituitary–adrenal responses to novel stress following repeated social stress using the resident/intruder paradigm. Horm Behav 43:158–165PubMedCrossRefGoogle Scholar
  3. Björkqvist K (2001) Social defeat as a stressor in humans. Physiol Behav 73:435–442PubMedCrossRefGoogle Scholar
  4. Brady KT, Dansky BS, Sonne SC, Saladin ME (1998) Posttraumatic stress disorder and cocaine dependence. Order of onset. Am J Addict 7:128–135PubMedGoogle Scholar
  5. Brown ZJ, Tribe E, D’souza NA, Erb S (2009) Interaction between noradrenaline and corticotrophin-releasing factor in the reinstatement of cocaine seeking in the rat. Psychopharmacology (Berl) 203:121–130CrossRefGoogle Scholar
  6. Bubar MJ, Cunningham KA (2008) Prospects for serotonin 5-HT2R pharmacotherapy in psychostimulant abuse. Prog Brain Res 172:319–346PubMedCrossRefGoogle Scholar
  7. Cador M, Bjijou Y, Stinus L (1995) Evidence of a complete independence of the neurobiological substrates for the induction and expression of behavioral sensitization to amphetamine. Neuroscience 65:385–395PubMedCrossRefGoogle Scholar
  8. Capriles N, Rodaros D, Sorge RE, Stewart J (2003) A role for the prefrontal cortex in stress- and cocaine-induced reinstatement of cocaine seeking in rats. Psychopharmacology (Berl) 168:66–74CrossRefGoogle Scholar
  9. Covington HE III, Miczek KA (2001) Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration “binges”. Psychopharmacology (Berl) 158:388–398CrossRefGoogle Scholar
  10. Covington HE III, Kikusui T, Goodhue J, Nikulina EM, Hammer RP Jr, Miczek KA (2005) Brief social defeat stress: long lasting effects on cocaine taking during a binge and zif268 mRNA expression in the amygdala and prefrontal cortex. Neuropsychopharmacology 30:310–321PubMedCrossRefGoogle Scholar
  11. Covington HE III, Tropea TF, Rajadhyaksha AM, Kosofsky BE, Miczek KA (2008) NMDA receptors in the rat VTA: a critical site for social stress to intensify cocaine taking. Psychopharmacology (Berl) 197:203–216CrossRefGoogle Scholar
  12. 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 Rev 15:71–100PubMedCrossRefGoogle Scholar
  13. Erb S, Shaham Y, Stewart J (1998) The role of corticotropin-releasing factor and corticosterone in stress- and cocaine-induced relapse to cocaine seeking in rats. J Neurosci 18:5529–5536PubMedGoogle Scholar
  14. Erb S, Petrovic A, Yi D, Kayyali H (2006) Central injections of CRF reinstate cocaine seeking in rats after postinjection delays of up to 3 h: an influence of time and environmental context. Psychopharmacology (Berl) 187:112–120CrossRefGoogle Scholar
  15. Goeders NE (2002) The HPA axis and cocaine reinforcement. Psychoneuroendocrinology 27:13–33PubMedCrossRefGoogle Scholar
  16. Goeders NE, Guerin GF (2000) Effects of the CRH receptor antagonist CP-154,526 on intravenous cocaine self-administration in rats. Neuropsychopharmacology 23:577–586PubMedCrossRefGoogle Scholar
  17. Gray TS (1993) Amygdaloid CRF pathways. Role in autonomic, neuroendocrine, and behavioral responses to stress. Ann NY Acad Sci 697:53–60PubMedCrossRefGoogle Scholar
  18. Higelin J, Py-Lang G, Paternoster C, Ellis GJ, Patel A, Dautzenberg FM (2001) 125I-Antisauvagine-30: a novel and specific high-affinity radioligand for the characterization of corticotropin-releasing factor type 2 receptors. Neuropharmacology 40:114–122PubMedCrossRefGoogle Scholar
  19. Iwasaki-Sekino A, Mano-Otagiri A, Ohata H, Yamauchi N, Shibasaki T (2009) Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological stress in rats. Psychoneuroendocrinology 34:226–237PubMedCrossRefGoogle Scholar
  20. Kalivas PW, Duffy P (1995) Selective activation of dopamine transmission in the shell of the nucleus accumbens by stress. Brain Res 675:325–328PubMedCrossRefGoogle Scholar
  21. Kalivas PW, Duffy P, Latimer LG (1987) Neurochemical and behavioral effects of corticotropin-releasing factor in the ventral tegmental area of the rat. J Pharmacol Exp Ther 242:757–763PubMedGoogle Scholar
  22. Le AD, Harding S, Juzytsch W, Watchus J, Shalev U, Shaham Y (2000) The role of corticotropin-releasing factor instress-induced relapse to alcohol-seeking behavior in rats. Psychopharmacology (Berl) 150:317–324CrossRefGoogle Scholar
  23. Lewis DA, Foote SL, Cha CI (1989) Corticotropin-releasing factor immunoreactivity in monkey neocortex: an immunohistochemical analysis. J Comp Neurol 290:599–613PubMedCrossRefGoogle Scholar
  24. Liu X, Weiss F (2002) Additive effect of stress and drug cues on reinstatement of ethanol seeking: exacerbation by history of dependence and role of concurrent activation of corticotropin-releasing factor and opioid mechanisms. J Neurosci 22:7856–7861PubMedGoogle Scholar
  25. Lodge DJ, Grace AA (2005) Acute and chronic corticotropin-releasing factor 1 receptor blockade inhibits cocaine-induced dopamine release: correlation with dopamine neuron activity. J Pharmacol Exp Ther 314:201–206PubMedCrossRefGoogle Scholar
  26. Makino S, Hashimoto K, Gold PW (2002) Multiple feedback mechanisms activating corticotropin-releasing hormone system in the brain during stress. Pharmacol Biochem Behav 73:147–158PubMedCrossRefGoogle Scholar
  27. Mansbach RS, Brooks EN, Chen YL (1997) Antidepressant-like effects of CP-154,526, a selective CRF1 receptor antagonist. Eur J Pharmacol 323:21–26PubMedCrossRefGoogle Scholar
  28. Marinelli M, Piazza PV (2002) Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur J Neurosci 16:387–394PubMedCrossRefGoogle Scholar
  29. McFarland K, Davidge SB, Lapish CC, Kalivas PW (2004) Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J Neurosci 24:1551–1560PubMedCrossRefGoogle Scholar
  30. Miczek KA (1979) A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine. Psychopharmacology (Berl) 60:253–259CrossRefGoogle Scholar
  31. Miczek KA, Mutschler NH (1996) Activational effects of social stress on IV cocaine self-administration in rats. Psychopharmacology (Berl) 128:256–264CrossRefGoogle Scholar
  32. Miczek KA, Yap JJ, Covington HE III (2008) Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake. Pharmacol Ther 120:102–128PubMedCrossRefGoogle Scholar
  33. Millan MA, Jacobowitz DM, Hauger RL, Catt KJ, Aguilera G (1986) Distribution of corticotropin-releasing factor receptors in primate brain. Proc Natl Acad Sci USA 83:1921–1925PubMedCrossRefGoogle Scholar
  34. Moghaddam B (2002) Stress activation of glutamate neurotransmission in the prefrontal cortex: implications for dopamine-associated psychiatric disorders. Biol Psychiatry 51:775–787PubMedCrossRefGoogle Scholar
  35. Müller MB, Wurst W (2004) Getting closer to affective disorders: the role of CRH receptor systems. Trends Mol Med 10:409–415PubMedCrossRefGoogle Scholar
  36. Nikulina EM, Covington HE III, Ganschow L, Hammer RP Jr, Miczek KA (2004) Long-term behavioral and neuronal cross-sensitization to amphetamine induced by repeated brief social defeat stress: Fos in the ventral tegmental area and amygdala. Neuroscience 123:857–865PubMedCrossRefGoogle Scholar
  37. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, 3rd edn. Academic, San DiegoGoogle Scholar
  38. Phillips PE, Stuber GD, Heien ML, Wightman RM, Carelli RM (2003) Subsecond dopamine release promotes cocaine seeking. Nature 422:614–618PubMedCrossRefGoogle Scholar
  39. Remie R, van Dongen JJ, Rensema JW (1990) Permanent cannulation of the jugular vein (acc. to Steffens). In: van Dongen JJ (ed) Manual of microsurgery on the laboratory rat. Elsevier, Amsterdam, pp 159–169Google Scholar
  40. Reyes BA, Valentino RJ, Van Bockstaele EJ (2008) Stress-induced intracellular trafficking of corticotropin-releasing factor receptors in rat locus coeruleus neurons. Endocrinology 149:122–130PubMedCrossRefGoogle Scholar
  41. Richardson NR, Roberts DCS (1996) Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J Neurosci Methods 66:1–11PubMedCrossRefGoogle Scholar
  42. Risbrough VB, Hauger RL, Pelleymounter MA, Geyer MA (2003) Role of corticotropin releasing factor (CRF) receptors 1 and 2 in CRF-potentiated acoustic startle in mice. Psychopharmacology (Berl) 170:178–187CrossRefGoogle Scholar
  43. Risbrough VB, Hauger RL, Roberts AL, Vale WW, Geyer MA (2004) Corticotropin-releasing factor receptors CRF1 and CRF2 exert both additive and opposing influences on defensive startle behavior. J Neurosci 24:6545–6552PubMedCrossRefGoogle Scholar
  44. Risbrough VB, Geyer MA, Hauger RL, Coste S, Stenzel-Poore M, Wurst W, Holsboer F (2009) CRF1 and CRF2 receptors are required for potentiated startle to contextual but not discrete cues. Neuropsychopharmacology 34:1494–1503PubMedCrossRefGoogle Scholar
  45. Rodaros D, Caruana DA, Amir S, Stewart J (2007) Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area. Neuroscience 150:8–13PubMedCrossRefGoogle Scholar
  46. Sakanaka M, Shibasaki T, Lederis K (1986) Distribution and efferent projections of corticotropin-releasing factor-like immunoreactivity in the rat amygdaloid complex. Brain Res 382:213–238PubMedCrossRefGoogle Scholar
  47. Sauvage M, Steckler T (2001) Detection of corticotropin-releasing hormone receptor 1 immunoreactivity in cholinergic, dopaminergic and noradrenergic neurons of the murine basal forebrain and brainstem nuclei-potential implication for arousal and attention. Neuroscience 104:643–652PubMedCrossRefGoogle Scholar
  48. Sawchenko PE, Imaki T, Potter E, Kovacs K, Imaki J, Vale W (1993) The functional neuroanatomy of corticotropin-releasing factor. Ciba Found Symp 172:5–21PubMedGoogle Scholar
  49. Schulz DW, Mansbach RS, Sprouse J, Braselton JP, Collins J, Corman M, Dunaiskis A, Faraci S, Schmidt AW, Seeger T, Seymour P, Tingley FD III, Winston EN, Chen YL, Heym J (1996) CP-154,526: a potent and selective nonpeptide antagonist of corticotropin releasing factor receptors. Proc Natl Acad Sci USA 93:10477–10482PubMedCrossRefGoogle Scholar
  50. Shaham Y, Funk D, Erb S, Brown TJ, Walker C, Stewart J (1997) Corticotropin-releasing factor, but not corticosterone, is involved in stress-induced relapse to heroin-seeking in rats. J Neurosci 17:0–4Google Scholar
  51. Shaham Y, Erb S, Leung S, Buczek Y, Stewart J (1998) CP-154,526, a selective, non-peptide antagonist of the corticotropin-releasing factor1 receptor attenuates stress-induced relapse to drug seeking in cocaine- and heroin-trained rats. Psychopharmacology (Berl) 137:184–190CrossRefGoogle Scholar
  52. Sinha R (2009) Stress and addiction: a dynamic interplay of genes, environment, and drug intake. Biol Psychiatry 66:100–101PubMedCrossRefGoogle Scholar
  53. Sinha R, Garcia M, Paliwal P, Kreek MJ, Rounsaville BJ (2006) Stress-induced cocaine craving and hypothalamic–pituitary–adrenal responses are predictive of cocaine relapse outcomes. Arch Gen Psychiatry 63:324–331PubMedCrossRefGoogle Scholar
  54. Specio SE, Wee S, O’Dell LE, Boutrel B, Zorrilla EP, Koob GF (2008) CRF(1) receptor antagonists attenuate escalated cocaine self-administration in rats. Psychopharmacology (Berl) 196:473–482CrossRefGoogle Scholar
  55. Substance Abuse and Mental Health Services Administration (2010) Results from the 2009 National Survey on Drug Use and Health: Volume I. Summary of national findings. US Department of Health and Human Services, RockvilleGoogle Scholar
  56. Swanson LW, Sawchenko PE, Rivier J, Vale WW (1983) Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36:165–186PubMedCrossRefGoogle Scholar
  57. 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 506:616–626PubMedCrossRefGoogle Scholar
  58. Tidey JW, Miczek KA (1996) Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res 721:140–149PubMedCrossRefGoogle Scholar
  59. Tornatzky W, Miczek KA (1995) Alcohol, anxiolytics and social stress in rats. Psychopharmacology (Berl) 121:135–144CrossRefGoogle Scholar
  60. 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 39:401–407PubMedCrossRefGoogle Scholar
  61. Valentino RJ, Van BE (2008) Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur J Pharmacol 583:194–203PubMedCrossRefGoogle Scholar
  62. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, Sawchenko PE (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428:191–212PubMedCrossRefGoogle Scholar
  63. Wanat MJ, Hopf FW, Stuber GD, Phillips PE, Bonci A (2008) Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J Physiol 586:2157–2170PubMedCrossRefGoogle Scholar
  64. Wang HL, Morales M (2008) Corticotropin-releasing factor binding protein within the ventral tegmental area is expressed in a subset of dopaminergic neurons. J Comp Neurol 509:302–318PubMedCrossRefGoogle Scholar
  65. 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 25:5389–5396PubMedCrossRefGoogle Scholar
  66. Wang B, You ZB, Rice KC, Wise RA (2007) Stress-induced relapse to cocaine seeking: roles for the CRF2 receptor and CRF-binding protein in the ventral tegmental area of the rat. Psychopharmacology (Berl) 193:283–294CrossRefGoogle Scholar
  67. Wang B, You ZB, Wise RA (2009) Reinstatement of cocaine seeking by hypocretin (orexin) in the ventral tegmental area: independence from the local corticotropin-releasing factor network. Biol Psychiatry 65:857–862PubMedCrossRefGoogle Scholar
  68. Wolf ME, Xue CJ, White FJ, Dahlin SL (1994) MK-801 does not prevent acute stimulatory effects of amphetamine or cocaine on locomotor activity or extracellular dopamine levels in rat nucleus accumbens. Brain Res 666:223–231PubMedCrossRefGoogle Scholar
  69. Yap JJ, Covington HE III, Gale MC, Datta R, Miczek KA (2005) Behavioral sensitization due to social defeat stress in mice: antagonism at mGluR5 and NMDA receptors. Psychopharmacology (Berl) 179:230–239CrossRefGoogle Scholar
  70. Zislis G, Desai TV, Prado M, Shah HP, Bruijnzeel AW (2007) Effects of the CRF receptor antagonist D-Phe CRF(12–41) and the alpha2-adrenergic receptor agonist clonidine on stress-induced reinstatement of nicotine-seeking behavior in rats. Neuropharmacology 53:958–966PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Christopher O. Boyson
    • 1
  • Tarciso T. Miguel
    • 2
  • Isabel M. Quadros
    • 3
  • Joseph F. DeBold
    • 1
  • Klaus A. Miczek
    • 1
  1. 1.Department of PsychologyTufts UniversityMedfordUSA
  2. 2.UFSCar/UNESP-AraraquaraAraraquaraBrazil
  3. 3.Universidade Federal de São Paulo (UNIFESP)São PauloBrazil

Personalised recommendations