Involvement of neural substrates in reward and aversion to methamphetamine addiction: Testing the reward comparison hypothesis and the paradoxical effect hypothesis of abused drugs
•The Cg1, IL, PrL, BLA, NAc, and DG probably mediated the paradoxical effect—reward and aversion.•Rewarding and aversive neural substrates involve in methamphetamine’s conditioned suppression.•Our data conflict the reward comparison but support the paradoxical effect hypothesis of abused drugs.•The...
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| Published in | Neurobiology of learning and memory Vol. 166; p. 107090 |
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| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
01.12.2019
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| Abstract | •The Cg1, IL, PrL, BLA, NAc, and DG probably mediated the paradoxical effect—reward and aversion.•Rewarding and aversive neural substrates involve in methamphetamine’s conditioned suppression.•Our data conflict the reward comparison but support the paradoxical effect hypothesis of abused drugs.•The findings provide some clinical insights for drug addiction.
Clinical studies of drug addiction focus on the reward impact of abused drugs that produces compulsive drug-seeking behavior and drug dependence. However, a small amount of research has examined the opposite effect of aversion to abused drugs to balance the reward effect for drug taking. An aversive behavioral model of abused drugs in terms of conditioned taste aversion (CTA) was challenged by the reward comparison hypothesis (Grigson, 1997). To test the reward comparison hypothesis, the present study examined the rewarding or aversive neural substrates involved in methamphetamine-induced conditioned suppression. The behavioral data showed that methamphetamine induced conditioned suppression on conditioning and reacquisition but extinguished it on extinction. A higher level of stressful aversive corticosterone occurred on conditioning and reacquisition but not extinction. The c-Fos or p-ERK immunohistochemical activity showed that the cingulated cortex area 1 (Cg1), infralimbic cortex (IL), prelimbic cortex (PrL), basolateral amygdala (BLA), nucleus accumbens (NAc), and dentate gyrus (DG) of the hippocampus were overexpressed in aversive CTA induced by methamphetamine. These data may indicate that the Cg1, IL, PrL, BLA, NAc, and DG probably mediated the paradoxical effect—reward and aversion. Altogether, our data conflicted with the reward comparison hypothesis, and methamphetamine may simultaneously induce the paradoxical effect of reward and aversion in the brain to support the paradoxical effect hypothesis of abused drugs. The present data implicate some insights for drug addiction in clinical aspects. |
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| AbstractList | Clinical studies of drug addiction focus on the reward impact of abused drugs that produces compulsive drug-seeking behavior and drug dependence. However, a small amount of research has examined the opposite effect of aversion to abused drugs to balance the reward effect for drug taking. An aversive behavioral model of abused drugs in terms of conditioned taste aversion (CTA) was challenged by the reward comparison hypothesis (Grigson, 1997). To test the reward comparison hypothesis, the present study examined the rewarding or aversive neural substrates involved in methamphetamine-induced conditioned suppression. The behavioral data showed that methamphetamine induced conditioned suppression on conditioning and reacquisition but extinguished it on extinction. A higher level of stressful aversive corticosterone occurred on conditioning and reacquisition but not extinction. The c-Fos or p-ERK immunohistochemical activity showed that the cingulated cortex area 1 (Cg1), infralimbic cortex (IL), prelimbic cortex (PrL), basolateral amygdala (BLA), nucleus accumbens (NAc), and dentate gyrus (DG) of the hippocampus were overexpressed in aversive CTA induced by methamphetamine. These data may indicate that the Cg1, IL, PrL, BLA, NAc, and DG probably mediated the paradoxical effect-reward and aversion. Altogether, our data conflicted with the reward comparison hypothesis, and methamphetamine may simultaneously induce the paradoxical effect of reward and aversion in the brain to support the paradoxical effect hypothesis of abused drugs. The present data implicate some insights for drug addiction in clinical aspects. •The Cg1, IL, PrL, BLA, NAc, and DG probably mediated the paradoxical effect—reward and aversion.•Rewarding and aversive neural substrates involve in methamphetamine’s conditioned suppression.•Our data conflict the reward comparison but support the paradoxical effect hypothesis of abused drugs.•The findings provide some clinical insights for drug addiction. Clinical studies of drug addiction focus on the reward impact of abused drugs that produces compulsive drug-seeking behavior and drug dependence. However, a small amount of research has examined the opposite effect of aversion to abused drugs to balance the reward effect for drug taking. An aversive behavioral model of abused drugs in terms of conditioned taste aversion (CTA) was challenged by the reward comparison hypothesis (Grigson, 1997). To test the reward comparison hypothesis, the present study examined the rewarding or aversive neural substrates involved in methamphetamine-induced conditioned suppression. The behavioral data showed that methamphetamine induced conditioned suppression on conditioning and reacquisition but extinguished it on extinction. A higher level of stressful aversive corticosterone occurred on conditioning and reacquisition but not extinction. The c-Fos or p-ERK immunohistochemical activity showed that the cingulated cortex area 1 (Cg1), infralimbic cortex (IL), prelimbic cortex (PrL), basolateral amygdala (BLA), nucleus accumbens (NAc), and dentate gyrus (DG) of the hippocampus were overexpressed in aversive CTA induced by methamphetamine. These data may indicate that the Cg1, IL, PrL, BLA, NAc, and DG probably mediated the paradoxical effect—reward and aversion. Altogether, our data conflicted with the reward comparison hypothesis, and methamphetamine may simultaneously induce the paradoxical effect of reward and aversion in the brain to support the paradoxical effect hypothesis of abused drugs. The present data implicate some insights for drug addiction in clinical aspects. |
| ArticleNumber | 107090 |
| Author | Huang, Andrew Chih Wei He, Alan Bo Han Liu, Yu Qin Kozłowska, Anna Chen, Jun Chien Wu, Chi-Wen Huang, Chung Lei |
| Author_xml | – sequence: 1 givenname: Alan Bo Han surname: He fullname: He, Alan Bo Han organization: Department of Psychology, Fo Guang University, Yilan County 26247, Taiwan – sequence: 2 givenname: Chung Lei surname: Huang fullname: Huang, Chung Lei organization: Department of Psychology, Fo Guang University, Yilan County 26247, Taiwan – sequence: 3 givenname: Anna surname: Kozłowska fullname: Kozłowska, Anna organization: Department of Human Physiology, School Medicine, Collegium Medicum, University of Warmia and Mazury in Olsztyn, Warszawska Av, 30, 10-082 Olsztyn, Poland – sequence: 4 givenname: Jun Chien surname: Chen fullname: Chen, Jun Chien organization: Department of Substance Abuse and Psychiatry, Tri-Service General Hospital Beitou Branch, Taipei 11243, Taiwan – sequence: 5 givenname: Chi-Wen surname: Wu fullname: Wu, Chi-Wen organization: Department of Psychology, Fo Guang University, Yilan County 26247, Taiwan – sequence: 6 givenname: Andrew Chih Wei surname: Huang fullname: Huang, Andrew Chih Wei email: chweihuang@mail.fgu.edu.tw organization: Department of Psychology, Fo Guang University, Yilan County 26247, Taiwan – sequence: 7 givenname: Yu Qin surname: Liu fullname: Liu, Yu Qin organization: Department of Psychology, Fo Guang University, Yilan County 26247, Taiwan |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31521799$$D View this record in MEDLINE/PubMed |
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| Keywords | c-Fos Neural substrates Reward Aversion p-ERK Methamphetamine |
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article-title: Brain activation in response to craving- and aversion-inducing cues related to alcohol in patients with alcohol dependence publication-title: Drug and Alcohol Dependence doi: 10.1016/j.drugalcdep.2014.05.017 contributor: fullname: Kim – volume: 16 start-page: 279 issue: 5 year: 2009 ident: 10.1016/j.nlm.2019.107090_b0320 article-title: Extinction circuits for fear and addiction overlap in prefrontal cortex publication-title: Learning & Memory doi: 10.1101/lm.1041309 contributor: fullname: Peters – volume: 101 start-page: 129 issue: 2 year: 1999 ident: 10.1016/j.nlm.2019.107090_b0290 article-title: Localization of brain reinforcement mechanisms: Intracranial self-administration and intracranial place-conditioning studies publication-title: Behavioural Brain Research doi: 10.1016/S0166-4328(99)00022-4 contributor: fullname: McBride |
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| SubjectTerms | Aversion c-Fos Methamphetamine Neural substrates p-ERK Reward |
| Title | Involvement of neural substrates in reward and aversion to methamphetamine addiction: Testing the reward comparison hypothesis and the paradoxical effect hypothesis of abused drugs |
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