The encoding of cocaine vs. natural rewards in the striatum of nonhuman primates: categories with different activations

Opriş, Ioan; Hampson, Robert E.; Deadwyler, Sam A.

doi:10.1016/j.neuroscience.2009.06.002

Cited by 43 publications

(49 citation statements)

References 65 publications

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“…encoding of stimulus-reward associations (18,19) and cue-induced reward expectation (20,21). Human functional neuroimaging data also demonstrate ventral striatal activity to cue presentation following appetitive and aversive Pavlovian conditioning (22).…”

Section: Discussionmentioning

confidence: 94%

Dorsolateral caudate nucleus differentiates cocaine from natural reward-associated contextual cues

Liu

Chefer

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Chronic drug administration induces neuroplastic changes within brain circuits regulating cognitive control and/or emotions. Following repeated pairings between drug intake and environmental cues, increased sensitivity to or salience of these contextual cues provoke conscious or unconscious craving and enhance susceptibility to relapse. To explore brain circuits participating in such experienceinduced plasticity, we combined functional MRI with a preclinical drug vs. food self-administration (SA) withdrawal model. Specifically, two groups of rats were trained to associate odor cues with the availability of i.v. cocaine or oral sucrose, respectively. After 20 d of cocaine or sucrose SA followed by prolonged (30 d) forced abstinence, animals were presented with odor cues previously associated with or without (S+/S−) reinforcer (cocaine/sucrose) availability while undergoing functional MRI scans. ANOVA results demonstrate that a learning effect distinguishing S+ from S− was seen in the insula and nucleus accumbens, with the insula response reflecting the individual history of cocaine SA intake. A main effect of group, distinguishing cocaine from sucrose, was seen in the medial prefrontal cortex (infralimbic, prelimbic, and cingulate cortex) and dorsolateral striatum. Critically, only the dorsomedial striatum demonstrated a double dissociation between the two SA groups and learning (S+ vs. S−). These findings demonstrate altered cortico-limbic-striatal reward-related processing to learned, environment reward-associated contextual odor cues, which may serve as potential biomarkers for therapeutic interventions.context cues | neuroplasticity | drug addiction P reventing or reducing the incidence of relapse remains the major challenge for the treatment of addiction, as recidivism rates can range as high as 90%. Both preclinical (1) and human addiction studies (2) have demonstrated that following repeated pairings with drug administration, various contextual and environmental stimuli when subsequently presented alone can elicit drug-seeking and drug-taking behaviors. Further, dysregulation within specific brain circuits regulating cognitive control and/or emotional regulation (3) can amplify the perceived salience of environmental contexts and cues that provoke craving (4) and thereby enhance susceptibility to relapse (2). These observations speak to the important role of reward learning in addictive processes (5). As such, it is critical to better understand the neural mechanisms and circuitry underlying the retrieval of cue-induced memories as an important intermediary in developing more efficacious interventions to decrease recidivism.The amygdala, nucleus accumbens (NAc), and various prefrontal cortical regions respond to drug-associated cues in human cocaine addicts (6, 7). Supporting their critical roles in the neural circuitry of drug-seeking behavior, these regions have also been identified using preclinical reinstatement models (8, 9). For example, NAc neurons exhibit conditioned responses to drugassociated env...

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Section: Discussionmentioning

confidence: 94%

Dorsolateral caudate nucleus differentiates cocaine from natural reward-associated contextual cues

Liu

Chefer

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…This drug-induced effect of intravenous cocaine is in accord with the involvement of the dorsal striatum in reward and addiction 57 . Importantly, striatal DA release has been shown to differentially activate subpopulations of striatal neurons 50, 58 , and cocaine is well known to elicit neural activity in the region 59, 60 . Overall, the data demonstrate that glucose influx follows electrically stimulated and pharmacologically evoked DA release, likely in response to metabolic demand within the dorsal striatum.…”

Section: Resultsmentioning

confidence: 99%

“…Separate investigations conducted in rats have shown that cocaine administration consistently increases CBF 64–66 and tissue oxygenation 66 in many brain regions, including the striatum. Furthermore, cocaine reward has been shown to increase cell firing in both the dorsal and ventral striatum of non-human primates 60 . The simultaneous measurements of glucose and DA at a single recording site reported herein are the first of their kind.…”

Section: Resultsmentioning

confidence: 99%

Simultaneous Voltammetric Measurements of Glucose and Dopamine Demonstrate the Coupling of Glucose Availability with Increased Metabolic Demand in the Rat Striatum

Smith

Lee

Dausch

et al. 2017

ACS Chem. Neurosci.

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Cerebral blood flow ensures delivery of nutrients, such as glucose, to brain sites with increased metabolic demand. However, little is known about rapid glucose dynamics at discrete locations during neuronal activation in vivo. Acute exposure to many substances of abuse elicits dopamine release and neuronal activation in the striatum; however, the concomitant changes in striatal glucose remain largely unknown. Recent developments have combined fast-scan cyclic voltammetry with glucose oxidase enzyme modified carbon-fiber microelectrodes to enable the measurement of glucose dynamics with subsecond temporal resolution in the mammalian brain. This work evaluates several waveforms to enable the first simultaneous detection of endogenous glucose and dopamine at single recording sites. These molecules, one electroactive and one non-electroactive, were found to fluctuate in the dorsal striatum in response to electrical stimulation of the midbrain and systemic infusion of cocaine/ raclopride. The data reveal the second-by-second dynamics of these species in a striatal microenvironment, and directly demonstrate the coupling of glucose availability with increased metabolic demand. This work provides a foundation that will enable detailed investigation of local mechanisms that regulate the coupling of cerebral blood flow with metabolic demand under normal conditions, and in animal studies of drug abuse and addiction.

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“…This finding, and our subsequent Daun02 inactivation results, support the hypothesis that during drug self-administration training, specific patterns of sparsely distributed neurons are selected by drug-associated contexts to form neuronal ensembles that encode learned associations between the contexts and drug effects (Cruz et al, 2013). In vivo electrophysiological recordings of single neurons during self-administration also suggest that different accumbens neurons are selectively activated by specific drug-associated contexts (and discrete cues) (Carelli et al, 1993;Peoples and West, 1996;Deadwyler et al, 2004;Opris et al, 2009;Guillem et al, 2013).…”

Section: Role Of Accumbens Shell Neuronal Ensembles In Contextinducedmentioning

confidence: 99%

Role of Nucleus Accumbens Shell Neuronal Ensembles in Context-Induced Reinstatement of Cocaine-Seeking

et al. 2014

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Environmental contexts previously associated with drug use provoke relapse to drug use in humans and reinstatement of drug seeking in animal models of drug relapse. We examined whether context-induced reinstatement of cocaine seeking is mediated by activation of context-selected nucleus accumbens neurons. We trained rats to self-administer cocaine in Context A and extinguished their lever-pressing in a distinct Context B. On test day, reexposure to the cocaine-associated Context A reinstated cocaine seeking and increased expression of the neural activity marker Fos in 3.3% of accumbens shell and 1.6% of accumbens core neurons. To assess a causal role for these activated neurons, we used the Daun02 inactivation procedure to selectively inactivate these neurons. We trained c-fos-lacZ transgenic rats to self-administer cocaine in Context A and extinguished their lever-pressing in Context B. On induction day, we exposed rats to either Context A or a novel Context C for 30 min and injected Daun02 or vehicle into accumbens shell or core 60 min later. On test day, 3 d after induction day, the ability of Context A to reinstate cocaine seeking and increase neuronal activity in accumbens shell was attenuated when Daun02 was previously injected after exposure to Context A. Daun02 injections after exposure to the novel Context C had no effect on context-induced reinstatement of cocaine seeking despite much greater numbers of Fos-expressing neurons induced by Context C. Daun02 injections in accumbens core had no effect. Our data suggest that context-induced reinstatement of cocaine seeking is mediated by activation of context-selected accumbens shell but not core neuronal ensembles.

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The encoding of cocaine vs. natural rewards in the striatum of nonhuman primates: categories with different activations

Cited by 43 publications

References 65 publications

Dorsolateral caudate nucleus differentiates cocaine from natural reward-associated contextual cues

Dorsolateral caudate nucleus differentiates cocaine from natural reward-associated contextual cues

Simultaneous Voltammetric Measurements of Glucose and Dopamine Demonstrate the Coupling of Glucose Availability with Increased Metabolic Demand in the Rat Striatum

Role of Nucleus Accumbens Shell Neuronal Ensembles in Context-Induced Reinstatement of Cocaine-Seeking

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