nach oben

Brain Structure and Function

Erschienen in:

01.09.2014 | Original Article

Mesoaccumbens dopamine signaling alteration underlies behavioral transition from tolerance to sensitization to morphine rewarding properties during morphine withdrawal

verfasst von: Linlin Sun, Ling Hu, Yijing Li, Cailian Cui

Erschienen in: Brain Structure and Function | Ausgabe 5/2014

Einloggen, um Zugang zu erhalten

Abstract

Although the firing activity of dopamine (DA) neurons in the ventral tegmental area (VTA) and the behavioral response to morphine rewarding properties alter as opiate withdrawal, little is known about the dynamic changes in DA signal pathway from the VTA to the nucleus accumbens (NAc) during prolonged withdrawal, and whether the changes are indicative of vulnerability to relapse of drug abuse. Here we report that morphine spontaneously withdrawn (SW) rats are incapable of responding to small dose of morphine-induced conditioned place preference (CPP) from 24h-SW to 30d-SW, but recover response at 45d-SW. Interestingly, mesoaccumbens DA signaling, including the firing of DA neurons in the VTA, contents of DA and its metabolic ratio, and the membrane level of dopamine D₁ receptor in the NAc elicited by morphine challenge, display a similar pattern of time-dependent changes during morphine withdrawal. Moreover, blockade of D₁ receptor abolishes this behavioral transition. In addition, a strong correlation was found between % change in CPP score and membrane D₁ receptor level induced by morphine challenge. These results indicate a time-dependent behavioral switch from tolerance to sensitization during the prolonged withdrawal, which could offer a window for therapeutic intervention via manipulations of D₁ receptors.

Nur mit Berechtigung zugänglich

Acquas E, Di Chiara G (1992) Depression of mesolimbic dopamine transmission and sensitization to morphine during opiate abstinence. J Neurochem 58(5):1620–1625PubMedCrossRef

Ahmed SH, Walker JR, Koob GF (2000) Persistent increase in the motivation to take heroin in rats with a history of drug escalation. Neuropsychopharmacology 22(4):413–421PubMedCrossRef

Bardo MT, Rowlett JK, Harris MJ (1995) Conditioned place preference using opiate and stimulant drugs: a meta-analysis. Neurosci Biobehav Rev 19(1):39–51PubMedCrossRef

Bonci A, Williams JT (1997) Increased probability of GABA release during withdrawal from morphine. J Neurosci 17(2):796–803PubMed

Chartoff EH, Mague SD, Carlezon Jr WA (2003) Effect of dopamine D1 receptor agonists on precipitated opiate withdrawal-induced place aversions in rats. Society for Neuroscience Abstract Viewer and Itinerary Planner 2003: Abstract No. 110.119

Chartoff EH, Barhight MF, Mague SD, Sawyer AM, Carlezon WA (2009) Anatomically dissociable effects of dopamine D1 receptor agonists on reward and relief of withdrawal in morphine-dependent rats. Psychopharmacology 204(2):227–239PubMedCentralPubMedCrossRef

Chergui K, Suaudchagny MF, Gonon F (1994) Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat-brain in vivo. Neuroscience 62(3):641–645PubMedCrossRef

Chiodo LA (1988) Dopamine-containing neurons in the mammalian central nervous system—electrophysiology and pharmacology. Neurosci Biobehav Rev 12(1):49–91PubMedCrossRef

Chu NN, Zuo YF, Meng L, Lee DYW, Han JS, Cui CL (2007) Peripheral electrical stimulation reversed the cell size reduction and increased BDNF level in the ventral tegmental area in chronic morphine-treated rats. Brain Res 1182:90–98PubMedCentralPubMedCrossRef

Chu NN, Xia W, Yu P, Hu L, Zhang R, Cui CL (2008) Chronic morphine-induced neuronal morphological changes in the ventral tegmental area in rats are reversed by electroacupuncture treatment. Addict Biol 13(1):47–51PubMedCrossRef

Di Chiara G (1999) Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 375(1–3):13–30PubMedCrossRef

Di Chiara G, North RA (1992) Neurobiology of opiate abuse. Trends Pharmacol Sci 13(5):185–193PubMedCrossRef

Diana M, Pistis M, Muntoni A, Gessa G (1995) Profound decrease of mesolimbic dopaminergic neuronal activity in morphine withdrawn rats. J Pharmacol Exp Ther 272(2):781–785PubMed

Dobi A, Margolis EB, Wang HL, Harvey BK, Morales M (2010) Glutamatergic and nonglutamatergic neurons of the ventral tegmental area establish local synaptic contacts with dopaminergic and nondopaminergic neurons. J Neurosci 30(1):218–229PubMedCentralPubMedCrossRef

Fields HL, Hjelmstad GO, Margolis EB, Nicola SM (2007) Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30:289–316PubMedCrossRef

Georges F, Aston-Jones G (2002) Activation of ventral tegmental area cells by the bed nucleus of the stria terminalis: a novel excitatory amino acid input to midbrain dopamine neurons. J Neurosci 22(12):5173–5187PubMed

Georges F, Le Moine C, Aston-Jones G (2006) No effect of morphine on ventral tegmental dopamine neurons during withdrawal. J Neurosci 26(21):5720–5726PubMedCrossRef

Gonon FG (1988) Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic-neurons as studied by in vivo electrochemistry. Neuroscience 24(1):19–28PubMedCrossRef

Grace AA, Bunney BS (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons.1. Identification and characterization. Neuroscience 10(2):301–315PubMedCrossRef

Grimm JW, Lu L, Hayashi T, Hope BT, Su TP, Shaham Y (2003) Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J Neurosci 23(3):742–747PubMed

Guyenet PG, Aghajanian GK (1978) Antidromic identification of dopaminergic and other output neurons of rat substantia nigra. Brain Res 150(1):69–84PubMedCrossRef

Gysling K, Wang RY (1983) Morphine-induced activation of a10 dopamine neurons in the rat. Brain Res 277(1):119–127PubMedCrossRef

Herz A (1998) Opioid reward mechanisms: a key role in drug abuse? Can J Physiol Pharmacol 76(3):252–258PubMedCrossRef

Hu L, Chu NN, Sun LL, Zhang R, Han JS, Cui CL (2009) Electroacupuncture treatment reverses morphine-induced physiological changes in dopaminergic neurons within the ventral tegmental area. Addict Biol 14(4):431–437PubMedCrossRef

Kalivas PW, Stewart J (1991) Dopamine transmission in the initiation and expression of drug-induced and stress-induced sensitization of motor-activity. Brain Res Rev 16(3):223–244PubMedCrossRef

Kenny PJ, Chen SA, Kitamura O, Markou A, Koob GF (2006) Conditioned withdrawal drives heroin consumption and decreases reward sensitivity. J Neurosci 26(22):5894–5900PubMedCrossRef

Koo JW, Mazei-Robison MS, Chaudhury D, Juarez B, LaPlant Q, Ferguson D, Feng J, Sun H, Scobie KN, Damez-Werno D, Crumiller M, Ohnishi YN, Ohnishi YH, Mouzon E, Dietz DM, Lobo MK, Neve RL, Russo SJ, Han M-H, Nestler EJ (2012) BDNF is a negative modulator of morphine action. Science 338(6103):124–128PubMedCentralPubMedCrossRef

Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24(2):97–129PubMedCrossRef

Koob GF, Le Moal M (2005) Plasticity of reward neurocircuitry and the ‘dark side’ of drug addiction. Nat Neurosci 8(11):1442–1444PubMedCrossRef

Laviolette SR, Nader K, van der Kooy D (2002) Motivational state determines the functional role of the mesolimbic dopamine system in the mediation of opiate reward processes. Behav Brain Res 129(1–2):17–29PubMedCrossRef

Lu L, Grimm JW, Hope BT, Shaham Y (2004) Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology 47:214–226PubMedCrossRef

Ma YY, Chu NN, Guo CY, Han JS, Cui CL (2007) NR2B-containing NMDA receptor is required for morphine-but not stress-induced reinstatement. Exp Neurol 203(2):309–319PubMedCrossRef

Ma YY, Meng L, Guo CY, Han JS, Lee DY, Cui CL (2009) Dose- and time-dependent, context-induced elevation of dopamine and its metabolites in the nucleus accumbens of morphine-induced CPP rats. Behav Brain Res 204(1):192–199PubMedCrossRef

Manzanedo C, Aguilar MA, Rodriguez-Arias M, Minarro J (2005) Sensitization to the rewarding effects of morphine depends on dopamine. Neuroreport 16(2):201–205PubMedCrossRef

Manzoni OJ, Williams JT (1999) Presynaptic regulation of glutamate release in the ventral tegmental area during morphine withdrawal. J Neurosci 19(15):6629–6636PubMed

Mazei-Robison MS, Koo JW, Friedman AK, Lansink CS, Robison AJ, Vinish M, Krishnan V, Kim S, Siuta MA, Galli A, Niswender KD, Appasani R, Horvath MC, Neve RL, Worley PF, Snyder SH, Hurd YL, Cheer JF, Han MH, Russo SJ, Nestler EJ (2011) Role for mTOR signaling and neuronal activity in morphine-induced adaptations in ventral tegmental area dopamine neurons. Neuron 72(6):977–990PubMedCentralPubMedCrossRef

Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, New York

Pothos E, Rada P, Mark GP, Hoebel BG (1991) Dopamine microdialysis in the nucleus accumbens during acute and chronic morphine, naloxone-precipitated withdrawal and clonidine treatment. Brain Res 566(1–2):348–350PubMedCrossRef

Rossetti ZL, Hmaidan Y, Gessa GL (1992) Marked inhibition of mesolimbic dopamine release: a common feature of ethanol, morphine, cocaine and amphetamine abstinence in rats. Eur J Pharmacol 221(2–3):227–234PubMedCrossRef

Russo SJ, Bolanos CA, Theobald DE, DeCarolis NA, Renthal W, Kumar A, Winstanley CA, Renthal NE, Wiley MD, Self DW, Russell DS, Neve RL, Eisch AJ, Nestler EJ (2007) IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat Neurosci 10(1):93–99PubMedCrossRef

Schultz W (2002) Getting formal with dopamine and reward. Neuron 36(2):241–263PubMedCrossRef

Shi XD, Wang GB, Ma YY, Ren W, Luo F, Cui CL, Han JS (2004) Repeated peripheral electrical stimulations suppress both morphine-induced CPP and reinstatement of extinguished CPP in rats: accelerated expression of PPE and PPD mRNA in NAc implicated. Brain Res Mol Brain Res 130(1–2):124–133PubMedCrossRef

Shippenberg TS, Emmettoglesby MW, Ayesta FJ, Herz A (1988) Tolerance and selective cross-tolerance to the motivational effects of opioids. Psychopharmacology 96(1):110–115PubMedCrossRef

Shippenberg TS, Bals-Kubik R, Herz A (1993) Examination of the neurochemical substrates mediating the motivational effects of opioids: role of the mesolimbic dopamine system and D-1 vs. D-2 dopamine receptors. J Pharmacol Exp Ther 265(1):53–59PubMed

Shippenberg TS, Heidbreder C, Lefevour A (1996) Sensitization to the conditioned rewarding effects of morphine: pharmacology and temporal characteristics. Eur J Pharmacol 299(1–3):33–39PubMedCrossRef

Shippenberg TS, LeFevour A, Thompson AC (1998) Sensitization to the conditioned rewarding effects of morphine and cocaine: differential effects of the kappa-opioid receptor agonist U69593. Eur J Pharmacol 345(1):27–34PubMedCrossRef

Sklair-Tavron L, Shi WX, Lane SB, Harris HW, Bunney BS, Nestler EJ (1996) Chronic morphine induces visible changes in the morphology of mesolimbic dopamine neurons. Proc Natl Acad Sci USA 93(20):11202–11207PubMedCentralPubMedCrossRef

Sterling P, Eyer J (1988) Allostasis: a new paradigm to explain arousal pathology. In: Fisher S, Reason J (eds) Handbook of life stress, cognition and health, vol xxxiii. Wiley, Oxford, England, pp 629–649

Sun W (2011) Dopamine neurons in the ventral tegmental area: drug-induced synaptic plasticity and its role in relapse to drug-seeking behavior. Curr Drug Abuse Rev 4(4):270–285PubMedCrossRef

Teismann P, Ferger B (2001) Inhibition of the cyclooxygenase isoenzymes COX-1 and COX-2 provide neuroprotection in the MPTP-mouse model of Parkinson’s disease. Synapse 39(2):167–174PubMedCrossRef

Tepper JM, Young SJ, Groves PM (1984) Autoreceptor-mediated changes in dopaminergic terminal excitability—effects of increases in impulse flow. Brain Res 309(2):309–316PubMedCrossRef

Thiblin I, Finn A, Ross SB, Stenfors C (1999) Increased dopaminergic and 5-hydroxytryptaminergic activities in male rat brain following long-term treatment with anabolic androgenic steroids. Br J Pharmacol 126(6):1301–1306PubMedCentralPubMedCrossRef

Ungless MA, Magill PJ, Bolam JP (2004) Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303(5666):2040–2042PubMedCrossRef

Willins DL, Meltzer HY (1998) Serotonin 5-HT2C agonists selectively inhibit morphine-induced dopamine efflux in the nucleus accumbens. Brain Res 781(1–2):291–299PubMedCrossRef

Titel: Mesoaccumbens dopamine signaling alteration underlies behavioral transition from tolerance to sensitization to morphine rewarding properties during morphine withdrawal
verfasst von: Linlin Sun
Ling Hu
Yijing Li
Cailian Cui
Publikationsdatum: 01.09.2014
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 5/2014
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-013-0599-2

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar "Chronische Unterbauch- und Viszeralschmerzen in der Praxis managen"

Springer Medizin

Mesoaccumbens dopamine signaling alteration underlies behavioral transition from tolerance to sensitization to morphine rewarding properties during morphine withdrawal

Abstract

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Stuhltransfusion könnte Fortschreiten von Parkinson-Symptomen bremsen

Frühe Tranexamsäure-Therapie nützt wenig bei Hirnblutungen

Sind Frauen die fähigeren Ärzte?

Akuter Schwindel: Wann lohnt sich eine MRT?

Update Neurologie

Live-Webinar "Chronische Unterbauch- und Viszeralschmerzen in der Praxis managen"

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 5/2014

Alterations of dendritic protrusions over the first postnatal year of a mouse: an analysis in layer VI of the barrel cortex

Developmental dyscalculia: a dysconnection syndrome?

Quantitative mapping of the local and extrinsic sources of GABA and Reelin to the layer Ia neuropil in the adult rat neocortex

Ultrastructure and synaptic connectivity of main and accessory olfactory bulb efferent projections terminating in the rat anterior piriform cortex and medial amygdala

Parvalbumin-immunoreactive neurons in the human claustrum

A direct anterior cingulate pathway to the primate primary olfactory cortex may control attention to olfaction

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Stuhltransfusion könnte Fortschreiten von Parkinson-Symptomen bremsen

Frühe Tranexamsäure-Therapie nützt wenig bei Hirnblutungen

Sind Frauen die fähigeren Ärzte?

Akuter Schwindel: Wann lohnt sich eine MRT?

Update Neurologie