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Psychopharmacology

, Volume 191, Issue 4, pp 899–907 | Cite as

The effects of a single session of inescapable tailshock on the subsequent locomotor response to brief footshock and cocaine administration in rats

  • Andre Der-AvakianEmail author
  • Robert R. Rozeske
  • Sondra T. Bland
  • Linda R. Watkins
  • Steven F. Maier
Original Investigation

Abstract

Rationale

We have previously shown that exposure to a single session of inescapable (IS), but not escapable (ES), tailshock can sensitize the subsequent conditioned place preference and locomotor responses to opioids, but not other drug classes. However, prior work suggests that IS might sensitize nonopioid drug responding if the drug were to be preceded by a mild stressor.

Objectives

In the following experiments, we examined the effects of IS and ES on the subsequent locomotor response to brief footshock and/or cocaine administration.

Methods

First, we measured the locomotor response to cocaine (0, 1, 5, 10 mg/kg, intraperitoneally) 48 h after a single session of IS in adult, male Sprague–Dawley rats. Then, this procedure was repeated with 10 mg/kg cocaine, except that half of the rats received two footshocks immediately before drug administration. Finally, we manipulated the escapability of the initial stressor, as rats received either ES or yoked IS 48 h prior to footshock and cocaine administration.

Results

IS did not affect the subsequent locomotor response to cocaine, but did enhance this response when cocaine administration was immediately preceded by two footshocks. The footshocks alone were without effect. This sensitizing effect was dependent on the escapability of the initial stressor, as ES did not alter the locomotor response to footshock and cocaine administration.

Conclusions

These results indicate that acute exposure to IS, but not ES, can sensitize the locomotor response to cocaine 48 h later, but only when cocaine administration is immediately preceded by a brief stressor.

Keywords

Reward Addiction Uncontrollable stress Inescapable shock Cocaine Psychostimulant Psychomotor Locomotor Sensitization Rat 

References

  1. Adinoff B (2004) Neurobiologic processes in drug reward and addiction. Harv Rev Psychiatry 12:305–320PubMedCrossRefGoogle Scholar
  2. Amat J, Matus-Amat P, Watkins LR, Maier SF (1998a) Escapable and inescapable stress differentially alter extracellular levels of 5-HT in the basolateral amygdala of the rat. Brain Res 812:113–120PubMedCrossRefGoogle Scholar
  3. Amat J, Matus-Amat P, Watkins LR, Maier SF (1998b) Escapable and inescapable stress differentially and selectively alter extracellular levels of 5-HT in the ventral hippocampus and dorsal periaqueductal gray of the rat. Brain Res 797:12–22PubMedCrossRefGoogle Scholar
  4. Berridge KC, Robinson TE (2003) Parsing reward. Trends Neurosci 26:507–513PubMedCrossRefGoogle Scholar
  5. Bland ST, Twining C, Schmid MJ, Der-Avakian A, Watkins LR, Maier SF (2004) Stress potentiation of morphine-induced dopamine efflux in the nucleus accumbens shell is dependent upon stressor uncontrollability and is mediated by the dorsal raphe nucleus. Neuroscience 126:705–715PubMedCrossRefGoogle Scholar
  6. Broderick PA, Phelix CF (1997) I. Serotonin (5-HT) within dopamine reward circuits signals open-field behavior. II. Basis for 5-HT-DA interaction in cocaine dysfunctional behavior. Neurosci Biobehav Rev 21:227–260PubMedCrossRefGoogle Scholar
  7. Covington HE 3rd, 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
  8. Cunningham KA, Lakoski JM (1988) Electrophysiological effects of cocaine and procaine on dorsal raphe serotonin neurons. Eur J Pharmacol 148:457–462PubMedCrossRefGoogle Scholar
  9. Cunningham KA, Lakoski JM (1990) The interaction of cocaine with serotonin dorsal raphe neurons. Single-unit extracellular recording studies. Neuropsychopharmacology 3:41–50PubMedGoogle Scholar
  10. De Deurwaerdere P, Stinus L, Spampinato U (1998) Opposite change of in vivo dopamine release in the rat nucleus accumbens and striatum that follows electrical stimulation of dorsal raphe nucleus: role of 5-HT3 receptors. J Neurosci 18:6528–6538PubMedGoogle Scholar
  11. del Rosario CN, Pacchioni AM, Cancela LM (2002) Influence of acute or repeated restraint stress on morphine-induced locomotion: involvement of dopamine, opioid and glutamate receptors. Behav Brain Res 134:229–238PubMedCrossRefGoogle Scholar
  12. Der-Avakian A, Bland ST, Rozeske RR, Tamblyn JT, Hutchinson MR, Watkins LR, Maier SF (2006) Single exposure to uncontrollable stress potentiates the subsequent conditioned place preference response to oxycodone, but not cocaine or ethanol. Psychopharmacology (Berl) (in press)Google Scholar
  13. 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):227–241PubMedGoogle Scholar
  14. Everitt BJ, Wolf ME (2002) Psychomotor stimulant addiction: a neural systems perspective. J Neurosci 22:3312–3320PubMedGoogle Scholar
  15. Goeders NE, Guerin GF (1994) Non-contingent electric footshock facilitates the acquisition of intravenous cocaine self-administration in rats. Psychopharmacology (Berl) 114:63–70CrossRefGoogle Scholar
  16. Grahn RE, Will MJ, Hammack SE, Maswood S, McQueen MB, Watkins LR, Maier SF (1999) Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res 826:35–43PubMedCrossRefGoogle Scholar
  17. Haile CN, GrandPre T, Kosten TA (2001) Chronic unpredictable stress, but not chronic predictable stress, enhances the sensitivity to the behavioral effects of cocaine in rats. Psychopharmacology (Berl) 154:213–220CrossRefGoogle Scholar
  18. Han DD, Gu HH (2006) Comparison of the monoamine transporters from human and mouse in their sensitivities to psychostimulant drugs. BMC Pharmacol 6:6PubMedCrossRefGoogle Scholar
  19. Jacobsen LK, Southwick SM, Kosten TR (2001) Substance use disorders in patients with posttraumatic stress disorder: a review of the literature. Am J Psychiatry 158:1184–1190PubMedCrossRefGoogle Scholar
  20. Jolas T, Aghajanian GK (1997) Opioids suppress spontaneous and NMDA-induced inhibitory postsynaptic currents in the dorsal raphe nucleus of the rat in vitro. Brain Res 755:229–245PubMedCrossRefGoogle Scholar
  21. Kalivas PW (1993) Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res Brain Res Rev 18:75–113PubMedCrossRefGoogle Scholar
  22. Koob GF (1999) Stress, corticotropin-releasing factor, and drug addiction. Ann N Y Acad Sci 897:27–45PubMedCrossRefGoogle Scholar
  23. Koob GF, Nestler EJ (1997) The neurobiology of drug addiction. J Neuropsychiatry Clin Neurosci 9:482–497PubMedGoogle Scholar
  24. Lepsch LB, Gonzalo LA, Magro FJ, Delucia R, Scavone C, Planeta CS (2005) Exposure to chronic stress increases the locomotor response to cocaine and the basal levels of corticosterone in adolescent rats. Addict Biol 10:251–256PubMedCrossRefGoogle Scholar
  25. Lu L, Shepard JD, Scott Hall F, Shaham Y (2003) Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 27:457–491PubMedCrossRefGoogle Scholar
  26. Maier SF, Ryan SM, Barksdale CM, Kalin NH (1986) Stressor controllability and the pituitary–adrenal system. Behav Neurosci 100:669–674PubMedCrossRefGoogle Scholar
  27. Marinelli M, Le Moal M, Piazza PV (1996) Acute pharmacological blockade of corticosterone secretion reverses food restriction-induced sensitization of the locomotor response to cocaine. Brain Res 724:251–255PubMedCrossRefGoogle Scholar
  28. Miczek KA, Mutschler NH (1996) Activational effects of social stress on IV cocaine self-administration in rats. Psychopharmacology (Berl) 128:256–264CrossRefGoogle Scholar
  29. Miczek KA, Nikulina E, Kream RM, Carter G, Espejo EF (1999) Behavioral sensitization to cocaine after a brief social defeat stress: c-fos expression in the PAG. Psychopharmacology (Berl) 141:225–234CrossRefGoogle Scholar
  30. Nikulina EM, Marchand JE, Kream RM, Miczek KA (1998) Behavioral sensitization to cocaine after a brief social stress is accompanied by changes in fos expression in the murine brainstem. Brain Res 810:200–210PubMedCrossRefGoogle Scholar
  31. Pacchioni AM, Gioino G, Assis A, Cancela LM (2002) A single exposure to restraint stress induces behavioral and neurochemical sensitization to stimulating effects of amphetamine: involvement of NMDA receptors. Ann N Y Acad Sci 965:233–246PubMedCrossRefGoogle Scholar
  32. Penington NJ, Reiffenstein RJ (1986) Direct comparison of hallucinogenic phenethylamines and D-amphetamine on dorsal raphe neurons. Eur J Pharmacol 122:373–377PubMedCrossRefGoogle Scholar
  33. Piazza PV, Le Moal M (1997) Glucocorticoids as a biological substrate of reward: physiological and pathophysiological implications. Brain Res Brain Res Rev 25:359–372PubMedCrossRefGoogle Scholar
  34. Piazza PV, Le Moal M (1998) The role of stress in drug self-administration. Trends Pharmacol Sci 19:67–74PubMedCrossRefGoogle Scholar
  35. Pistis M, Muntoni AL, Gessa G, Diana M (1997) Effects of acute, chronic ethanol and withdrawal on dorsal raphe neurons: electrophysiological studies. Neuroscience 79:171–176PubMedCrossRefGoogle Scholar
  36. Rebec GV, Curtis SD (1983) Reciprocal changes in the firing rate of neostriatal and dorsal raphe neurons following local infusions or systemic injections of D-amphetamine: evidence for neostriatal heterogeneity. J Neurosci 3:2240–2250PubMedGoogle Scholar
  37. Rueter LE, Fornal CA, Jacobs BL (1997) A critical review of 5-HT brain microdialysis and behavior. Rev Neurosci 8:117–137PubMedGoogle Scholar
  38. Shaham Y, Kelsey JE, Stewart J (1995) Temporal factors in the effect of restraint stress on morphine-induced behavioral sensitization in the rat. Psychopharmacology (Berl) 117:102–109CrossRefGoogle Scholar
  39. Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158:343–359CrossRefGoogle Scholar
  40. Takase LF, Nogueira MI, Bland ST, Baratta M, Watkins LR, Maier SF, Fornal CA, Jacobs BL (2005) Effect of number of tailshocks on learned helplessness and activation of serotonergic and noradrenergic neurons in the rat. Behav Brain Res 162:299–306PubMedCrossRefGoogle Scholar
  41. Tao R, Auerbach SB (1995) Involvement of the dorsal raphe but not median raphe nucleus in morphine-induced increases in serotonin release in the rat forebrain. Neuroscience 68:553–561PubMedCrossRefGoogle Scholar
  42. Tao R, Auerbach SB (2002a) GABAergic and glutamatergic afferents in the dorsal raphe nucleus mediate morphine-induced increases in serotonin efflux in the rat central nervous system. J Pharmacol Exp Ther 303:704–710PubMedCrossRefGoogle Scholar
  43. Tao R, Auerbach SB (2002b) Opioid receptor subtypes differentially modulate serotonin efflux in the rat central nervous system. J Pharmacol Exp Ther 303:549–556PubMedCrossRefGoogle Scholar
  44. Thielen RJ, Morzorati SL, McBride WJ (2001) Effects of ethanol on the dorsal raphe nucleus and its projections to the caudate putamen. Alcohol 23:131–139PubMedCrossRefGoogle Scholar
  45. Will MJ, Watkins LR, Maier SF (1998) Uncontrollable stress potentiates morphine’s rewarding properties. Pharmacol Biochem Behav 60:655–664PubMedCrossRefGoogle Scholar
  46. Will MJ, Der-Avakian A, Pepin JL, Durkan BT, Watkins LR, Maier SF (2002) Modulation of the locomotor properties of morphine and amphetamine by uncontrollable stress. Pharmacol Biochem Behav 71:345–351PubMedCrossRefGoogle Scholar
  47. Will MJ, Der-Avakian A, Bland ST, Grahn RE, Hammack SE, Sparks PD, Pepin JL, Watkins LR, Maier SF (2004) Electrolytic lesions and pharmacological inhibition of the dorsal raphe nucleus prevent stressor potentiation of morphine conditioned place preference in rats. Psychopharmacology (Berl) 171:191–198CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Andre Der-Avakian
    • 1
    Email author
  • Robert R. Rozeske
    • 1
  • Sondra T. Bland
    • 1
  • Linda R. Watkins
    • 1
  • Steven F. Maier
    • 1
  1. 1.Department of Psychology and Center for NeuroscienceUniversity of ColoradoBoulderUSA

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