Role of Dorsomedial Striatum Neuronal Ensembles in Incubation of Methamphetamine Craving after Voluntary Abstinence

Caprioli, Daniele; Vènniro, Marco; Zhang, Michelle; Bossert, Jennifer M.; Warren, Brandon L.; Hope, Bruce T.; Shaham, Yavin

doi:10.1523/jneurosci.3091-16.2017

Cited by 40 publications

(85 citation statements)

References 5 publications

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“…β-Gal within the behaviorally activated neurons converts Daun02 into daunorubicin, which inactivates and ablates these neurons (30,32). This method has been used in recent studies on the role of striatal and cortical neuronal ensembles in conditioned drug effects and drug relapse (31,48–50), including relapse to nicotine seeking (51). …”

Section: Resultsmentioning

confidence: 99%

“…Although previous studies have demonstrated that neuronal ensembles in nucleus accumbens or prefrontal cortex mediate relapse to drug seeking (31,48,49,51), only a single drug memory (operant memory) was investigated. In the current study, we established an animal model of multiple drug memories (pavlovian and operant reward memories) and found that the different cue–drug associations are stored in different neuronal ensembles in BLA.…”

Section: Discussionmentioning

confidence: 99%

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Selective Inhibition of Amygdala Neuronal Ensembles Encoding Nicotine-Associated Memories Inhibits Nicotine Preference and Relapse

Xue

Chen

Zhang

et al. 2017

Biological Psychiatry

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BACKGROUND: Nicotine craving and relapse often occurs after reactivation of nicotine reward memories. We recently developed a memory retrieval–reconsolidation interference procedure in which reactivating nicotine reward memories by acute exposure to nicotine (the unconditioned stimulus [UCS]) and then pharmacologically interfering with memory reconsolidation decreased relapse to nicotine seeking in rats and nicotine craving in smokers. Here, we investigated underlying mechanisms. METHODS: In the first series of experiments, we trained rats for nicotine-induced conditioned place preference (CPP) or nicotine self-administration and ventricularly microinjected them with the protein synthesis inhibitor anisomycin immediately after UCS-induced memory retrieval. In the second series of experiments, we used tyramide-amplified immunohistochemistry–fluorescence in situ hybridization to examine neural ensembles in the basolateral amygdala (BLA) reactivated by nicotine conditioned stimulus– or UCS-induced memory retrieval. We then used the Daun02 chemogenetic inactivation procedure to selectively inhibit the nicotine UCS-reactivated BLA neuronal ensembles. RESULTS: Ventricular injections of the anisomycin immediately after nicotine UCS memory retrieval inhibited sub-sequent nicotine CPP and relapse to operant nicotine seeking after short or prolonged abstinence. More important, within BLA, distinct neuronal ensembles encoded pavlovian CPP and operant self-administration reward memories and nicotine (the UCS) injections in the home cage reactivated both neuronal ensembles. Daun02 chemogenetic inactivation of the nicotine-reactivated ensembles inhibited both nicotine CPP and relapse to nicotine seeking. CONCLUSIONS: Results demonstrate that the nicotine UCS-induced memory retrieval manipulation reactivates multiple nicotine reward memories that are encoded by distinct BLA neuronal ensembles that play a role in nicotine preference and relapse.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Selective Inhibition of Amygdala Neuronal Ensembles Encoding Nicotine-Associated Memories Inhibits Nicotine Preference and Relapse

Xue

Chen

Zhang

et al. 2017

Biological Psychiatry

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“…Based on the above-mentioned 'translational' considerations, we recently developed a rat model of incubation of methamphetamine craving after prolonged alternative reward choice-based voluntary abstinence (Caprioli et al, 2015a;Caprioli et al, 2016). Our model is based on studies showing that most rats strongly prefer the non-drug reward when given a mutually exclusive choice between cocaine or methamphetamine and palatable food (Cantin et al, 2010;Caprioli et al, 2015b;Lenoir et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Between tests, the rats underwent voluntary abstinence for 19 days (achieved via a mutually exclusive discrete choice procedure between methamphetamine and the palatable food in which, on any given trial, the rats can earn the food or drug reward but not both; 20 trials/day). Under our voluntary abstinence procedure, most rats achieve complete methamphetamine abstinence during most of the choice sessions (ie, zero choices of methamphetamine infusions), whereas some rats continue to occasionally self-administer a small number of drug infusions during these sessions (Caprioli et al, 2015a;Caprioli et al, 2016;Caprioli et al, 2015b) (see Figure 2). We found that under both training conditions, methamphetamine seeking in the extinction tests was higher after 21 abstinence days than after 1 day, demonstrating incubation of drug craving after voluntary abstinence.…”

Section: Introductionmentioning

confidence: 99%

Incubation of Methamphetamine but not Heroin Craving After Voluntary Abstinence in Male and Female Rats

Vènniro¹,

Zhang²,

Shaham³

et al. 2016

Neuropsychopharmacol

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115

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We recently introduced an animal model of incubation of methamphetamine craving after choice-based voluntary abstinence in male rats. Here we studied the generality of this phenomenon to (1) female rats, and (2) male and female rats with a history of heroin self-administration. We first trained rats to self-administer palatable food pellets for 6 days (6 h per day) for either methamphetamine (0.1 mg/kg/infusion) or heroin (0.1 mg/kg/infusion) for 12 days (6 h/day). We then assessed relapse to drug seeking under extinction conditions after 1 and 21 abstinence days. Between tests, the rats underwent either voluntary abstinence (achieved via a discrete choice procedure between drug and palatable food; 20 trials/day) or home-cage forced abstinence. We found no sex differences in methamphetamine self-administration or in the strong preference for the palatable food over methamphetamine during the choice-based voluntary abstinence. In both sexes, methamphetamine seeking in the relapse tests was higher after 21 days of either voluntary or forced abstinence than after 1 day (incubation of methamphetamine craving). We also found no sex differences in heroin self-administration or the strong preference for the palatable food over heroin during the choice-based voluntary abstinence. However, male and female rats with a history of heroin self-administration showed incubation of heroin craving after forced but not voluntary abstinence. Our results show that incubation of methamphetamine craving after voluntary abstinence generalizes to female rats. Unexpectedly, prolonged voluntary abstinence prevented the emergence of incubation of heroin craving in both sexes.

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“…Specifically, Fos-expressing neuronal ensembles are capable of representing highly specific associations based on patterns of activation and connectivity. Studies indicate about 5% or less of neurons in a histochemical section are Fos-expressing following most operant learned behaviors (Bossert et al, 2011; Fanous et al, 2013; Warren et al, 2016; Caprioli et al, 2017). These percentages of Fos-expressing neurons, quantified in two-dimensional histochemical slices, translate to less than 1% of neurons in three-dimensional brain volumes.…”

Section: Fos-expressing Neuronal Ensembles Are Capable Of High Mechanmentioning

confidence: 99%

Mechanistic Resolution Required to Mediate Operant Learned Behaviors: Insights from Neuronal Ensemble-Specific Inactivation

Warren

Suto

Hope

2017

Front. Neural Circuits

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Many learned behaviors are directed by complex sets of highly specific stimuli or cues. The neural mechanisms mediating learned associations in these behaviors must be capable of storing complex cue information and distinguishing among different learned associations—we call this general concept “mechanistic resolution”. For many years, our understanding of the circuitry of these learned behaviors has been based primarily on inactivation of specific cell types or whole brain areas regardless of which neurons were activated during the cue-specific behaviors. However, activation of all cells or specific cell types in a brain area do not have enough mechanistic resolution to encode or distinguish high-resolution learned associations in these behaviors. Instead, these learned associations are likely encoded within specific patterns of sparsely distributed neurons called neuronal ensembles that are selectively activated by the cues. This review article focuses on studies of neuronal ensembles in operant learned responding to obtain food or drug rewards. These studies suggest that the circuitry of operant learned behaviors may need to be re-examined using ensemble-specific manipulations that have the requisite level of mechanistic resolution.

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Role of Dorsomedial Striatum Neuronal Ensembles in Incubation of Methamphetamine Craving after Voluntary Abstinence

Abstract: We recently developed a rat model of incubation of methamphetamine craving after choice-based voluntary abstinence. Here, we studied the role of dorsolateral striatum (DLS) and dorsomedial striatum (DMS) in this incubation. We trained rats to selfadminister palatable food pellets (

Cited by 40 publications

References 5 publications

Selective Inhibition of Amygdala Neuronal Ensembles Encoding Nicotine-Associated Memories Inhibits Nicotine Preference and Relapse

Selective Inhibition of Amygdala Neuronal Ensembles Encoding Nicotine-Associated Memories Inhibits Nicotine Preference and Relapse

Incubation of Methamphetamine but not Heroin Craving After Voluntary Abstinence in Male and Female Rats

Mechanistic Resolution Required to Mediate Operant Learned Behaviors: Insights from Neuronal Ensemble-Specific Inactivation

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