A role for the prefrontal cortex in heroin-seeking after forced abstinence by adult male rats but not adolescents

Neuropsychopharmacology

Volumn 38, Issue 3, 2013, Pages 446-454

  Doherty, James M ^a   Cooke, Bradley M ^a   Frantz, Kyle J ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

c Fos; development; opiate; Periadolescent; reinstatement; relapse

Indexed keywords

DIAMORPHINE;

ADOLESCENT; AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENUATION; CONTROLLED STUDY; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; DRUG WITHDRAWAL; HEROIN DEPENDENCE; MALE; MEDIAL PREFRONTAL CORTEX; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; REINFORCEMENT; STEREOLOGY;

AGE FACTORS; ANIMALS; BEHAVIOR, ADDICTIVE; CONDITIONING, OPERANT; HEROIN; HEROIN DEPENDENCE; MALE; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SELF ADMINISTRATION;

EID: 84872485936     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.200     Document Type: Article

References (51)

1. Adriani W, Laviola G (2004). Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav Pharmacol 15: 341-352.
2. Andersen SL, Thompson AT, Rutstein M, Hostetter JC, Teicher MH (2000). Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37: 167-169.
3. Anker J, Carroll M (2010). Reinstatement of cocaine seeking induced by drugs, cues, and stress in adolescent and adult rats. Psychopharmacology (Berl) 208: 211-222.
4. Balda M, Anderson K, Itzhak Y (2006). Adolescent and adult responsiveness to the incentive value of cocaine reward in mice: role of neuronal nitric oxide synthase (nNOS) gene. Neuro-pharmacology 51: 341-349.
5. Bossert J, Stern A, Theberge FRM, Cifani C, Koya E, Hope B et al (2011). Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin. Nat Neurosci 14: 420-422.
6. Brenhouse H, Sonntag K, Andersen S (2008). Transient D1 dopamine receptor expression on prefrontal cortex projection neurons: relationship to enhanced motivational salience of drug cues in adolescence. J Neurosci 28: 2375-2382.
7. Brenhouse HC, Dumais K, Andersen SL (2010). Enhancing the salience of dullness: behavioral and pharmacological strategies to facilitate extinction of drug-cue associations in adolescent rats. Neuroscience 169: 628-636.
8. Caine S, Lintz R, Koob G(eds) (1993). Intravenous drug-self- administration techniques in animals. Oxford University Press: New York, NY.
9. Cao J, Lotfipour S, Loughlin S, Leslie F (2007). Adolescent maturation of cocaine-sensitive neural mechanisms. Neuropsychopharmacology 32: 2279-2289.
10. Caster JM, Kuhn CM (2009). Maturation of coordinated immediate early gene expression by cocaine during adolescence. Neuroscience 160: 13-31.
11. Chung T, Maisto SA (2006). Relapse to alcohol and other drug use in treated adolescents: review and reconsideration of relapse as a change point in clinical course. Clin Psychol Rev 26: 149-161.
12. Cooke BM (2011). Synaptic reorganisation of the medial amygdala during puberty. J Neuroendocrinol 23: 65-73.
13. Crews F, He J, Hodge C (2007). Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86: 189-199.
14. Doherty J, Frantz K (2012a). Heroin self-administration and reinstatement of heroin-seeking in adolescent vs. adult male rats. Psychopharmacology (Berl) 219: 763-773.
15. Doherty J, Frantz K (2012b). Attenuated effects of experimenter- administered heroin in adolescent vs. adult male rats: physical withdrawal and locomotor sensitization. Psychopharmacology (Berl); e-pub ahead of print 2 September 2012.
16. Doherty J, Ogbomnwan Y, Williams B, Frantz K (2009). Agedependent morphine intake and cue-induced reinstatement, but not escalation in intake, by adolescent and adult male rats. Pharmacol Biochem Behav 92: 164-172.
17. Doremus TL, Brunell SC, Varlinskaya EI, Spear LP (2003). Anxiogenic effects during withdrawal from acute ethanol in adolescent and adult rats. Pharmacol Biochem Behav 75: 411-418.
18. Ernst M, Fudge JL (2009). A developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes. Neurosci Biobehav Rev 33: 367-382.
19. Harlan RE, Garcia MM (1998). Drugs of abuse and immediate-early genes in the forebrain. Mol Neurobiol 16: 221-267.
20. Harvey R, Dembro K, Rajagopalan K, Mutebi M, Kantak K (2009). Effects of self-administered cocaine in adolescent and adult male rats on orbitofrontal cortex-related neurocognitive functioning. Psychopharmacology (Berl) 206: 61-71.
21. Hodgson SR, Hofford RS, Wellman PJ, Eitan S (2009). Different affective response to opioid withdrawal in adolescent and adult mice. Life Sci 84: 52-60.
22. Johnston LD, O'Malley PM, Bachman JG, Schulenberg JE (2010). Monitoring the Future national results on adolescent drug use: overview of key findings, 2009. NIH Publication No 10-7583.
23. Kalivas P, Volkow N (2005). The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162: 1403-1413.
24. Kandel DB, Yamaguchi K, Chen K (1992). Stages of progression in drug involvement from adolescence to adulthood: further evidence for the gateway theory. J Stud Alcohol 53: 447-457.
25. Kerstetter KA, Kantak KM (2007). Differential effects of self-administered cocaine in adolescent and adult rats on stimulus-reward learning. Psychopharmacology (Berl) 194: 403-411.
26. Koya E, Spijker S, Voorn P, Binnekade R, Schmidt ED, Schoffelmeer AN et al (2006). Enhanced cortical and accumbal molecular reactivity associated with conditioned heroin, but not sucrose-seeking behaviour. J Neurochem 98: 905-915.
27. Kuntz K, Patel K, Grigson P, Freeman W, Vrana K (2008). Heroin self-administration: II. CNS gene expression following with-drawal and cue-induced drug-seeking behavior. Pharmacol Biochem Behav 90: 349-356.
28. Lenroot R, Giedd J (2006). Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci Biobehav Rev 30: 718-729.
29. Li C, Frantz KJ (2009). Attenuated incubation of cocaine seeking in male rats trained to self-administer cocaine during periadoles-cence. Psychopharmacology (Berl) 204: 725-733.
30. Markham JA, Morris JR, Juraska JM (2007). Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood. Neuroscience 144: 961-968.
31. Mouton P (2002). The Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists. Johns Hopkins University Press: Baltimore, MD.
32. Nestler EJ (2001). Molecular basis of long-term plasticity under-lying addiction. Nature Rev Neurosci 2: 119-128.
33. O'Dell LE, Bruijnzeel AW, Smith RT, Parsons LH, Merves ML, Goldberger BA et al (2006). Diminished nicotine withdrawal in adolescent rats: implications for vulnerability to addiction. Psychopharmacology (Berl) 186: 612-619.
34. O'Brien CP (1997). A range of research-based pharmacotherapies for addiction. Science 278: 66-70.
35. Palmer RH, Young SE, Hopfer CJ, Corley RP, Stallings MC, Crowley TJ et al (2009). Developmental epidemiology of drug use and abuse in adolescence and young adulthood: Evidence of generalized risk. Drug Alcohol Depend 102: 78-87.
36. Paxinos G, Watson C (1998). The rat brain in stereotaxic coordinates. 4th edn Academic Press: San Diego, CA.
37. Peters J, Kalivas P, Quirk G (2009). Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16: 279-288.
38. Robinson TE, Gorny G, Savage VR, Kolb B (2002). Widespread but regionally specific effects of experimenter- versus self-administered morphine on dendritic spines in the nucleus accumbens, hippocampus, and neocortex of adult rats. Synapse 46: 271-279.
39. SAMHSA (2012). Substance Abuse and Mental Health Services Administration, results from the 2010 National Survey on Drug Use and Health: National Findings, NSDUH Series H-42, HHS. SAMHSA: Rockville, MD, Publication No. (SMA) 11-4667.
40. Schochet T, Kelley A, Landry C (2004). Differential behavioral effects of nicotine exposure in adolescent and adult rats. Psychopharmacology (Berl) 175: 265-273.
41. Schochet TL, Kelley AE, Landry CF (2005). Differential expression of arc mRNA and other plasticity-related genes induced by nicotine in adolescent rat forebrain. Neuroscience 135: 285-297.
42. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003). The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168: 3-20.
43. Shahbazi M, Moffett AM, Williams BF, Frantz KJ (2008). Age- and sex-dependent amphetamine self-administration in rats. Psycho-pharmacology (Berl) 196: 71-81.
44. Shalev U, Morales M, Hope B, Yap J, Shaham Y (2001). Time-dependent changes in extinction behavior and stress-induced reinstatement of drug seeking following withdrawal from heroin in rats. Psychopharmacology (Berl) 156: 98-107.
45. Shram M, Funk D, Li Z, Lê AD (2007). Acute nicotine enhances c-fos mRNA expression differentially in reward-related sub-strates of adolescent and adult rat brain. Neurosci Lett 418: 286-291.
46. Shram MJ, Funk D, Li Z, Lê AD (2008). Nicotine self-adminis- tration, extinction responding and reinstatement in adolescent and adult male rats: evidence against a biological vulner-ability to nicotine addiction during adolescence. Neuropsycho-pharmacology 33: 739-748.
47. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW (1999). In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 2: 859-861.
48. Spear LP (2000). The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24: 417-463.
49. Sturman DA, Moghaddam B (2011). Reduced neuronal inhibition and coordination of adolescent prefrontal cortex during motivated behavior. J Neurosci 31: 1471-1478.
50. Tseng K-Y, O'Donnell P (2007). Dopamine modulation of prefrontal cortical interneurons changes during adolescence. Cereb Cortex 17: 1235-1240.
51. Van den Oever M, Goriounova N, Li K, Van der Schors R, Binnekade R, Schoffelmeer ANM et al (2008). Prefrontal cortex AMPA receptor plasticity is crucial for cue-induced relapse to heroin-seeking. Nat Neurosci 11: 1053-1058.