Cocaine Experience Establishes Control of Midbrain Glutamate and Dopamine by Corticotropin-releasing Factor: a Role in Stress-induced Relapse to Drug Seeking

Overview

Journal J Neurosci

Specialty Neurology

Date 2005 Jun 3

PMID 15930388

Citations 212

Authors

Bin Wang

Yavin Shaham

Dawnya Zitzman

Soraya Azari

Roy A Wise

Zhi-Bing You

Affiliations

Soon will be listed here.

Abstract

Footshock stress can reinstate cocaine-seeking behavior through a central action of the stress-associated neurohormone corticotropin-releasing factor (CRF). Here we report (1) that footshock stress releases CRF in the ventral tegmental area (VTA) of the rat brain, (2) that, in cocaine-experienced but not in cocaine-naive rats, this CRF acquires control over local glutamate release, (3) that CRF-induced glutamate release activates the mesocorticolimbic dopamine system, and (4) that, through this circuitry, footshock stress triggers relapse to drug seeking in cocaine-experienced animals. Thus, a long-lasting cocaine-induced neuroadaptation, presumably at the level of glutamate terminals in the VTA, appears to play an important role in stress-induced relapse to drug use. Similar neuroadaptations may be important for the comorbidity between addiction and other stress-related psychiatric disorders.

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References

Legault M, Wise R . Injections of N-methyl-D-aspartate into the ventral hippocampus increase extracellular dopamine in the ventral tegmental area and nucleus accumbens. Synapse. 1999; 31(4):241-9. DOI: 10.1002/(SICI)1098-2396(19990315)31:4<241::AID-SYN1>3.0.CO;2-#. View

Erb S, Stewart J . A role for the bed nucleus of the stria terminalis, but not the amygdala, in the effects of corticotropin-releasing factor on stress-induced reinstatement of cocaine seeking. J Neurosci. 1999; 19(20):RC35. PMC: 6782764. View

Legault M, Rompre P, Wise R . Chemical stimulation of the ventral hippocampus elevates nucleus accumbens dopamine by activating dopaminergic neurons of the ventral tegmental area. J Neurosci. 2000; 20(4):1635-42. PMC: 6772387. View

Shaham Y, Erb S, Stewart J . Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Brain Res Rev. 2000; 33(1):13-33. DOI: 10.1016/s0165-0173(00)00024-2. View

Van Pett K, Viau V, Bittencourt J, Chan R, Li H, Arias C . Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol. 2000; 428(2):191-212. DOI: 10.1002/1096-9861(20001211)428:2<191::aid-cne1>3.0.co;2-u. View

Drevets W . Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression. Prog Brain Res. 2000; 126:413-31. DOI: 10.1016/S0079-6123(00)26027-5. View

Nestler E . Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci. 2001; 2(2):119-28. DOI: 10.1038/35053570. View

Sarnyai Z, Shaham Y, Heinrichs S . The role of corticotropin-releasing factor in drug addiction. Pharmacol Rev. 2001; 53(2):209-43. View

Ungless M, Whistler J, Malenka R, Bonci A . Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature. 2001; 411(6837):583-7. DOI: 10.1038/35079077. View

10.

Sauvage M, Steckler T . 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. 2001; 104(3):643-52. DOI: 10.1016/s0306-4522(01)00137-3. View

11.

Sinha R . How does stress increase risk of drug abuse and relapse?. Psychopharmacology (Berl). 2002; 158(4):343-59. DOI: 10.1007/s002130100917. View

12.

Erb S, Salmaso N, Rodaros D, Stewart J . A role for the CRF-containing pathway from central nucleus of the amygdala to bed nucleus of the stria terminalis in the stress-induced reinstatement of cocaine seeking in rats. Psychopharmacology (Berl). 2002; 158(4):360-5. DOI: 10.1007/s002130000642. View

13.

Moghaddam B . Stress activation of glutamate neurotransmission in the prefrontal cortex: implications for dopamine-associated psychiatric disorders. Biol Psychiatry. 2002; 51(10):775-87. DOI: 10.1016/s0006-3223(01)01362-2. View

14.

Leri F, Flores J, Rodaros D, Stewart J . Blockade of stress-induced but not cocaine-induced reinstatement by infusion of noradrenergic antagonists into the bed nucleus of the stria terminalis or the central nucleus of the amygdala. J Neurosci. 2002; 22(13):5713-8. PMC: 6758192. DOI: 20026536. View

15.

Capriles N, Rodaros D, Sorge R, Stewart J . A role for the prefrontal cortex in stress- and cocaine-induced reinstatement of cocaine seeking in rats. Psychopharmacology (Berl). 2002; 168(1-2):66-74. DOI: 10.1007/s00213-002-1283-z. View

16.

Saal D, Dong Y, Bonci A, Malenka R . Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron. 2003; 37(4):577-82. DOI: 10.1016/s0896-6273(03)00021-7. View

17.

Baker D, McFarland K, Lake R, Shen H, Tang X, Toda S . Neuroadaptations in cystine-glutamate exchange underlie cocaine relapse. Nat Neurosci. 2003; 6(7):743-9. DOI: 10.1038/nn1069. View

18.

Lu L, Grimm J, Shaham Y, Hope B . Molecular neuroadaptations in the accumbens and ventral tegmental area during the first 90 days of forced abstinence from cocaine self-administration in rats. J Neurochem. 2003; 85(6):1604-13. DOI: 10.1046/j.1471-4159.2003.01824.x. View

19.

Ungless M, Singh V, Crowder T, Yaka R, Ron D, Bonci A . Corticotropin-releasing factor requires CRF binding protein to potentiate NMDA receptors via CRF receptor 2 in dopamine neurons. Neuron. 2003; 39(3):401-7. DOI: 10.1016/s0896-6273(03)00461-6. View

20.

Herman J, Figueiredo H, Mueller N, Ulrich-Lai Y, Ostrander M, Choi D . Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol. 2003; 24(3):151-80. DOI: 10.1016/j.yfrne.2003.07.001. View