Activation in Extended Amygdala Corresponds to Altered Hedonic Processing During Protracted Morphine Withdrawal

Overview

Journal Behav Brain Res

Specialties Neurology
Psychology
Social Sciences

Date 2006 Nov 25

PMID 17123639

Citations 45

Authors

Glenda C Harris

Gary Aston-Jones

Affiliations

Soon will be listed here.

Abstract

Previously we reported that during protracted morphine abstinence rats show reduced conditioned place preferences (CPP) for food-associated environments, compared to non-dependent subjects. To determine the brain regions involved in this altered reward behavior, we examined neural activation (as indexed by Fos-like proteins) induced by a preference test for a food-associated environment in 5-week morphine-abstinent versus non-dependent animals. The results indicate that elevated Fos expression in the anterior cingulate cortex (Cg) and basolateral amygdala (BLA) correlated positively with preference behavior in all groups. In contrast, Fos expression in stress-associated brain areas, including the ventral lateral bed nucleus of the stria terminalis (VL-BNST), central nucleus of the amygdala (CE), and noradrenergic (A2) neurons in the nucleus tractus solitarius (NTS) was significantly elevated only in morphine-abstinent animals. Furthermore, the number of Fos positive neurons in these areas was found to correlate negatively with food preference in abstinent animals. These results indicate that the altered hedonic processing during protracted morphine withdrawal leading to decreased preference for cues associated with natural rewards may involve heightened activity in stress-related brain areas of the extended amygdala and their medullary noradrenergic inputs.

Citing Articles

Neuroplasticity of the extended amygdala in opioid withdrawal and prolonged opioid abstinence.

Kaplan G, Thompson B Front Pharmacol. 2023; 14:1253736.

PMID: 38044942 PMC: 10690374. DOI: 10.3389/fphar.2023.1253736.

Mu Opioid Receptor-Positive Neurons in the Dorsal Raphe Nucleus Are Impaired by Morphine Abstinence.

Welsch L, Colantonio E, Falconnier C, Champagnol-DiLiberti C, Allain F, Ben Hamida S Biol Psychiatry. 2023; 94(11):852-862.

PMID: 37393045 PMC: 10851617. DOI: 10.1016/j.biopsych.2023.06.024.

Acupuncture for protracted opioid abstinence syndrome: study protocol for a systematic review and meta-analysis.

Li T, Zeng Y, Zhang F, Zhou X, Ren Y BMJ Open. 2023; 13(6):e071864.

PMID: 37336541 PMC: 10314547. DOI: 10.1136/bmjopen-2023-071864.

Advances in the characterization of negative affect caused by acute and protracted opioid withdrawal using animal models.

Ozdemir D, Allain F, Kieffer B, Darcq E Neuropharmacology. 2023; 232:109524.

PMID: 37003572 PMC: 10844657. DOI: 10.1016/j.neuropharm.2023.109524.

Involvement of the Dorsal Vagal Complex in Alcohol-Related Behaviors.

Keller B, Hajnal A, Browning K, Arnold A, Silberman Y Front Behav Neurosci. 2022; 16:801825.

PMID: 35330845 PMC: 8940294. DOI: 10.3389/fnbeh.2022.801825.

References

Harris G, Aston-Jones G . Augmented accumbal serotonin levels decrease the preference for a morphine associated environment during withdrawal. Neuropsychopharmacology. 2000; 24(1):75-85. DOI: 10.1016/S0893-133X(00)00184-6. View

Markou A, Koob G . Postcocaine anhedonia. An animal model of cocaine withdrawal. Neuropsychopharmacology. 1991; 4(1):17-26. View

Gooley J, Schomer A, Saper C . The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat Neurosci. 2006; 9(3):398-407. DOI: 10.1038/nn1651. View

Myers E, Rinaman L . Viscerosensory activation of noradrenergic inputs to the amygdala in rats. Physiol Behav. 2003; 77(4-5):723-9. DOI: 10.1016/s0031-9384(02)00925-3. View

Barr A, Hofmann C, Weinberg J, Phillips A . Exposure to repeated, intermittent d-amphetamine induces sensitization of HPA axis to a subsequent stressor. Neuropsychopharmacology. 2002; 26(3):286-94. DOI: 10.1016/S0893-133X(01)00308-6. View

Walker D, Davis M . Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci. 1997; 17(23):9375-83. PMC: 6573581. View

Watkins S, Koob G, Markou A . Dramatic decreases in brain reward function during nicotine withdrawal. Nature. 1998; 393(6680):76-9. DOI: 10.1038/30001. View

Yoburn B, Chen J, Huang T, Inturrisi C . Pharmacokinetics and pharmacodynamics of subcutaneous morphine pellets in the rat. J Pharmacol Exp Ther. 1985; 235(2):282-6. View

Maldonado R . The neurobiology of addiction. J Neural Transm Suppl. 2003; (66):1-14. DOI: 10.1007/978-3-7091-0541-2_1. View

10.

Parkinson J, Cardinal R, Everitt B . Limbic cortical-ventral striatal systems underlying appetitive conditioning. Prog Brain Res. 2000; 126:263-85. DOI: 10.1016/S0079-6123(00)26019-6. View

11.

Chou T, Scammell T, Gooley J, Gaus S, Saper C, Lu J . Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J Neurosci. 2003; 23(33):10691-702. PMC: 6740926. View

12.

Zarrindast M, Ahmadi S, Haeri-Rohani A, Rezayof A, Jafari M, Jafari-Sabet M . GABA(A) receptors in the basolateral amygdala are involved in mediating morphine reward. Brain Res. 2004; 1006(1):49-58. DOI: 10.1016/j.brainres.2003.12.048. View

13.

Delfs J, Zhu Y, Druhan J, Aston-Jones G . Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion. Nature. 2000; 403(6768):430-4. DOI: 10.1038/35000212. View

14.

Elmquist J, Elias C, Saper C . From lesions to leptin: hypothalamic control of food intake and body weight. Neuron. 1999; 22(2):221-32. DOI: 10.1016/s0896-6273(00)81084-3. View

15.

Heinrichs S, Menzaghi F, Schulteis G, Koob G, Stinus L . Suppression of corticotropin-releasing factor in the amygdala attenuates aversive consequences of morphine withdrawal. Behav Pharmacol. 1995; 6(1):74-80. View

16.

Cardinal R, Parkinson J, Hall J, Everitt B . Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev. 2002; 26(3):321-52. DOI: 10.1016/s0149-7634(02)00007-6. View

17.

Delfs J, Zhu Y, Druhan J . Origin of noradrenergic afferents to the shell subregion of the nucleus accumbens: anterograde and retrograde tract-tracing studies in the rat. Brain Res. 1998; 806(2):127-40. DOI: 10.1016/s0006-8993(98)00672-6. View

18.

See R . Neural substrates of cocaine-cue associations that trigger relapse. Eur J Pharmacol. 2005; 526(1-3):140-6. DOI: 10.1016/j.ejphar.2005.09.034. View

19.

Koob G, Le Moal M . Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology. 2000; 24(2):97-129. DOI: 10.1016/S0893-133X(00)00195-0. View

20.

Barr A, Phillips A . Withdrawal following repeated exposure to d-amphetamine decreases responding for a sucrose solution as measured by a progressive ratio schedule of reinforcement. Psychopharmacology (Berl). 1999; 141(1):99-106. DOI: 10.1007/s002130050812. View