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  • 1.
    Fredriksson, Ida
    et al.
    Behavioral Neuroscience Branch, IRP/NIDA/NIH, Baltimore, MD, USA.
    Applebey, Sarah V
    Behavioral Neuroscience Branch, IRP/NIDA/NIH, Baltimore, MD.
    Minier-Toribio, Angelica
    Behavioral Neuroscience Branch, IRP/NIDA/NIH, Baltimore, MD.
    Shekara, Aniruddha
    Behavioral Neuroscience Branch, IRP/NIDA/NIH, Baltimore, MD.
    Bossert, Jennifer M.
    Behavioral Neuroscience Branch, IRP/NIDA/NIH, Baltimore, MD.
    Shaham, Yavin
    Behavioral Neuroscience Branch, IRP/NIDA/NIH, Baltimore, MD, USA.
    Effect of the dopamine stabilizer (-)-OSU6162 on potentiated incubation of opioid craving after electric barrier-induced voluntary abstinence.2020In: Neuropsychopharmacology, ISSN 0893-133X, E-ISSN 1740-634X, Vol. 45, no 5, p. 770-779Article in journal (Refereed)
    Abstract [en]

    In the classical incubation of drug craving rat model, drug seeking is assessed after homecage forced abstinence. However, human abstinence is often voluntary because negative consequences of drug seeking outweigh the desire for the drug. Here, we developed a rat model of incubation of opioid craving after electric barrier-induced voluntary abstinence and determined whether the dopamine stabilizer (-)-OSU6162 would decrease this new form of incubation. We trained male and female rats to self-administer oxycodone (0.1 mg/kg/infusion, 6 h/day) for 14 days. We then exposed them to either homecage forced abstinence or voluntary abstinence induced by an electric barrier of increasing intensity near the drug-paired lever. On abstinence days 1, 15, or 30, we tested the rats for oxycodone seeking without shock and drug. We also examined the effect of (-)-OSU6162 (7.5 and 15 mg/kg) on oxycodone seeking on abstinence day 1 or after 15 days of either voluntary or forced abstinence. Independent of sex, the time-dependent increase in oxycodone seeking after cessation of opioid self-administration (incubation of opioid craving) was stronger after voluntary abstinence than after forced abstinence. In males, (-)-OSU6162 decreased incubated (day 15) but not non-incubated (day 1) oxycodone seeking after either voluntary or forced abstinence. In females, (-)-OSU6162 modestly decreased incubated oxycodone seeking after voluntary but not forced abstinence. Results suggest that voluntary abstinence induced by negative consequences of drug seeking can paradoxically potentiate opioid craving and relapse. We propose the dopamine stabilizer (-)-OSU6162 may serve as an adjunct pharmacological treatment to prevent relapse in male opioid users.

  • 2.
    Fredriksson, Ida
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience. Linköping University, Faculty of Medicine and Health Sciences. NIDA, MD 21224 USA.
    Tsai, Pei-Jung
    NIDA, MD 21224 USA.
    Shekara, Aniruddha
    NIDA, MD 21224 USA.
    Duan, Ying
    NIDA, MD 21224 USA.
    Applebey, Sarah V
    NIDA, MD 21224 USA.
    Lu, Hanbing
    NIDA, MD 21224 USA.
    Bossert, Jennifer M.
    NIDA, MD 21224 USA.
    Shaham, Yavin
    NIDA, MD 21224 USA.
    Yang, Yihong
    NIDA, MD 21224 USA.
    Orbitofrontal cortex and dorsal striatum functional connectivity predicts incubation of opioid craving after voluntary abstinence2021In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 118, no 43, article id e2106624118Article in journal (Refereed)
    Abstract [en]

    We recently introduced a rat model of incubation of opioid craving after voluntary abstinence induced by negative consequences of drug seeking. Here, we used resting-state functional MRI to determine whether longitudinal functional connectivity changes in orbitofrontal cortex (OFC) circuits predict incubation of opioid craving after voluntary abstinence. We trained rats to self-administer for 14 d either intravenous oxycodone or palatable food. After 3 d, we introduced an electric barrier for 12 d that caused cessation of reward self-administration. We tested the rats for oxycodone or food seeking under extinction conditions immediately after selfadministration training (early abstinence) and after electric barrier exposure (late abstinence). We imaged their brains before selfadministration and during early and late abstinence. We analyzed changes in OFC functional connectivity induced by reward selfadministration and electric barrier-induced abstinence. Oxycodone seeking was greater during late than early abstinence (incubation of oxycodone craving). Oxycodone self-administration experience increased OFC functional connectivity with dorsal striatum and related circuits that was positively correlated with incubated oxycodone seeking. In contrast, electric barrier-induced abstinence decreased OFC functional connectivity with dorsal striatum and related circuits that was negatively correlated with incubated oxycodone seeking. Food seeking was greater during early than late abstinence (abatement of food craving). Food self-administration experience and electric barrier-induced abstinence decreased or maintained functional connectivity in these circuits that were not correlated with abated food seeking. Opposing functional connectivity changes in OFC with dorsal striatum and related circuits induced by opioid self-administration versus voluntary abstinence predicted individual differences in incubation of opioid craving.

  • 3.
    Fredriksson, Ida
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience. Linköping University, Faculty of Medicine and Health Sciences. NIDA, MD 21224 USA.
    Tsai, Pei-Jung
    NIDA, MD USA.
    Shekara, Aniruddha
    NIDA, MD 21224 USA.
    Duan, Ying
    NIDA, MD USA.
    Applebey, Sarah V.
    NIDA, MD 21224 USA.
    Minier-Toribio, Angelica
    NIDA, MD 21224 USA.
    Batista, Ashley
    NIDA, MD 21224 USA.
    Chow, Jonathan J.
    NIDA, MD 21224 USA.
    Altidor, Lindsay
    NIDA, MD 21224 USA.
    Barbier, Estelle
    Linköping University, Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience. Linköping University, Faculty of Medicine and Health Sciences.
    Cifani, Carlo
    Univ Camerino, Italy.
    Li, Xuan
    Univ Maryland, MD 20742 USA.
    Reiner, David J.
    NIDA, MD 21224 USA.
    Rubio, F. Javier
    NIDA, MD 21224 USA.
    Hope, Bruce T.
    NIDA, MD 21224 USA.
    Yang, Yihong
    NIDA, MD USA.
    Bossert, Jennifer M.
    NIDA, MD 21224 USA.
    Shaham, Yavin
    NIDA, MD 21224 USA.
    Role of ventral subiculum neuronal ensembles in incubation of oxycodone craving after electric barrier-induced voluntary abstinence2023In: Science Advances, E-ISSN 2375-2548, Vol. 9, no 2, article id eadd8687Article in journal (Refereed)
    Abstract [en]

    High relapse rate is a key feature of opioid addiction. In humans, abstinence is often voluntary due to negative consequences of opioid seeking. To mimic this human condition, we recently introduced a rat model of incubation of oxycodone craving after electric barrier-induced voluntary abstinence. Incubation of drug craving refers to time-dependent increases in drug seeking after cessation of drug self-administration. Here, we used the activity marker Fos, muscimol-baclofen (GABAa + GABAb receptor agonists) global inactivation, Daun020-selective inactivation of putative relapse-associated neuronal ensembles, and fluorescence-activated cell sorting of Fos-positive cells and quantitative polymerase chain reaction to demonstrate a key role of vSub neuronal ensembles in incubation of oxycodone craving after voluntary abstinence, but not homecage forced abstinence. We also used a longitudinal functional magnetic resonance imaging method and showed that functional connectivity changes in vSub-related circuits predict opioid relapse after abstinence induced by adverse consequences of opioid seeking.

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  • 4.
    Fredriksson, Ida
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience. Linköping University, Faculty of Medicine and Health Sciences. NIDA, MD 21224 USA.
    Venniro, Marco
    Linköping University, Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience. Linköping University, Faculty of Medicine and Health Sciences. NIDA, MD 21224 USA.
    Reiner, David J.
    Linköping University, Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience. Linköping University, Faculty of Medicine and Health Sciences. NIDA, MD 21224 USA.
    Chow, Jonathan J.
    Linköping University, Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience. Linköping University, Faculty of Medicine and Health Sciences. NIDA, MD 21224 USA.
    Bossert, Jennifer M.
    Linköping University, Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience. Linköping University, Faculty of Medicine and Health Sciences. NIDA, MD 21224 USA.
    Shaham, Yavin
    Linköping University, Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience. Linköping University, Faculty of Medicine and Health Sciences. NIDA, MD 21224 USA.
    Animal Models of Drug Relapse and Craving after Voluntary Abstinence: A Review2021In: Pharmacological Reviews, ISSN 0031-6997, E-ISSN 1521-0081, Vol. 73, no 3, p. 1050-1083Article, review/survey (Refereed)
    Abstract [en]

    Relapse to drug use during abstinence is a defining feature of addiction. During the last several decades, this clinical scenario has been studied at the preclinical level using classic relapse/reinstatement models in which drug seeking is assessed after experimenter-imposed home-cage forced abstinence or extinction of the drug-reinforced responding in the self-administration chambers. To date, however, results from studies using rat relapse/reinstatement models have yet to result in Food and Drug Administration-approved medications for relapse prevention. The reasons for this state of affairs are complex and multifaceted, but one potential reason is that, in humans, abstinence is often self-imposed or voluntary and occurs either because the negative consequences of drug use outweigh the drugs rewarding effects or because of the availability of nondrug alternative rewards that are chosen over the drug. Based on these considerations, we and others have recently developed rat models of relapse after voluntary abstinence, achieved either by introducing adverse consequences to drug taking (punishment) or seeking (electric barrier) or by providing mutually exclusive choices between the self-administered drug and nondrug rewards (palatable food or social interaction). In this review, we provide an overview of these translationally relevant relapse models and discuss recent neuropharmacological findings from studies using these models. We also discuss sex as a biological variable, future directions, and clinical implications of results from relapse studies using voluntary abstinence models. Our main conclusion is that the neuropharmacological mechanisms controlling relapse to drug seeking after voluntary abstinence are often different from the mechanisms controlling relapse after home-cage forced abstinence or reinstatement after extinction. Significance Statement-This review describes recently developed rat models of relapse after voluntary abstinence, achieved either by introducing adverse consequences to drug taking or seeking or by providing mutually exclusive choices between the self-administered drug and nondrug rewards. This review discusses recent neuropharmacological findings from studies using these models and discusses future directions and clinical implications.

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