Effects of Expectations for Different Reward Magnitudes on Neuronal Activity in Primate Striatum

Cromwell, Howard C.; Schultz, Wolfram

doi:10.1152/jn.01014.2002

Cited by 313 publications

(287 citation statements)

References 89 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: 96%

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: 96%

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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“…Afferent projections to the VS, like those to the dorsal striatum are derived from three major sources: a massive, generally topographic glutamatergic input from cerebral cortex; a large glutamatergic input from the thalamus; and a smaller, but critical input from the brainstem, primarily from the midbrain dopaminergic cells. Although this section primarily focuses on the connections of the VS, it gives some attention to the dorsal striatum, especially the caudate nucleus, an area that is also involved in reward-based learning (Cromwell and Schultz, 2003;Kennerley and Wallis, 2009;Watanabe and Hikosaka, 2005). This region receives input from the dPFC.…”

Section: Organization Of the Vsmentioning

confidence: 99%

The Reward Circuit: Linking Primate Anatomy and Human Imaging

Haber

Knutson

2009

Neuropsychopharmacol

3,175

193

2,859

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Although cells in many brain regions respond to reward, the cortical-basal ganglia circuit is at the heart of the reward system. The key structures in this network are the anterior cingulate cortex, the orbital prefrontal cortex, the ventral striatum, the ventral pallidum, and the midbrain dopamine neurons. In addition, other structures, including the dorsal prefrontal cortex, amygdala, hippocampus, thalamus, and lateral habenular nucleus, and specific brainstem structures such as the pedunculopontine nucleus, and the raphe nucleus, are key components in regulating the reward circuit. Connectivity between these areas forms a complex neural network that mediates different aspects of reward processing. Advances in neuroimaging techniques allow better spatial and temporal resolution. These studies now demonstrate that human functional and structural imaging results map increasingly close to primate anatomy.

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“…Other studies of electrophysiology and dopamine release in rats have also shown that both neuronal firing or dopamine release tend to signal the "better" of two reward options rather than their absolute value (Day et al, 2010;Roesch et al, 2007). Studies in monkeys have also tried to address whether striatal activations incorporate details of upcoming rewards and have demonstrated differences in activation patterns induced by two different types of juices (Hassani et al, 2001) as well as rewards of different magnitudes (Cromwell and Schultz, 2003). Finally, human neuroimaging studies have shown a specific relationship between BOLD signal increase in the NAc and magnitude of reward (Cooper and Knutson, 2008;Knutson and Cooper, 2005;Yacubian et al, 2006) and dichotomous activation for the cue predicting the greatest available reward value has also been observed (Ballard and Knutson, 2009).…”

Section: Nucleus Accumbens Activation and Reward Magnitude Codingmentioning

confidence: 99%

Changes in reward-related signals in the rat nucleus accumbens measured by in vivo oxygen amperometry are consistent with fMRI BOLD responses in man

et al. 2012

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a b s t r a c t a r t i c l e i n f oReal-time in vivo oxygen amperometry, a technique that allows measurement of regional brain tissue oxygen (O 2 ) has been previously shown to bear relationship to the BOLD signal measured with functional magnetic resonance imaging (fMRI) protocols. In the present study, O 2 amperometry was applied to the study of reward processing in the rat nucleus accumbens to validate the technique with a behavioural process known to cause robust signals in human neuroimaging studies. After acquisition of a cued-lever pressing task a robust increase in O 2 tissue levels was observed in the nucleus accumbens specifically following a correct lever press to the rewarded cue. This O 2 signal was modulated by cue reversal but not lever reversal, by differences in reward magnitudes and by the motivational state of the animal consistent with previous reports of the role of the nucleus accumbens in both the anticipation and representation of reward value. Moreover, this modulation by reward value was related more to the expected incentive value rather than the hedonic value of reward, also consistent with previous reports of accumbens coding of "wanting" of reward. Altogether, these results show striking similarities to those obtained in human fMRI studies suggesting the use of oxygen amperometry as a valid surrogate for fMRI in animals performing cognitive tasks, and a powerful approach to bridge between different techniques of measurement of brain function.

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Effects of Expectations for Different Reward Magnitudes on Neuronal Activity in Primate Striatum

Cited by 313 publications

References 89 publications

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

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

The Reward Circuit: Linking Primate Anatomy and Human Imaging

Changes in reward-related signals in the rat nucleus accumbens measured by in vivo oxygen amperometry are consistent with fMRI BOLD responses in man

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