Cocaine Seeking Habits Depend upon Dopamine-Dependent Serial Connectivity Linking the Ventral with the Dorsal Striatum

Belin, David; Everitt, Barry J.

doi:10.1016/j.neuron.2007.12.019

Cited by 645 publications

(556 citation statements)

References 60 publications

(87 reference statements)

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“…Although either manipulation on its own was without effect, the combined procedures selectively decreased cocaine seeking in extensively trained rats but not in rats that had undergone only moderate training (23). Together with our study, these findings underline the functional significance of the network interaction between the VMS and the DLS in drugrelated behavior.…”

Section: Dopamine Signaling In the Sensorimotor Striatum Emerges Beforesupporting

confidence: 79%

“…This progressive involvement of the DLS in drug seeking has been linked to circuitry that connects the VMS to the DLS by a serial disconnection study that demonstrated that the development of advanced cue-controlled drug-seeking behavior is dependent on intact VMS circuitry (23). Therefore, to test whether the later-emerging phasic dopamine signal in DLS reported in the present study was dependent upon antecedent activity in the VMS circuitry, we mimicked a disconnection of the VMS from DLS on one side of the brain with a unilateral excitotoxic lesion of the nucleus accumbens core (VMS) by infusing quinolinic acid before training (23), leaving the other side intact. Voltammetric microsensors were implanted bilaterally in the DLS (n = 17), permitting within-subject comparison of emergent DLS dopamine transmission between hemispheres, one hemisphere having an intact and the other a lesioned VMS (see Fig.…”

Section: Dopamine Receptors In the Dls Are Necessary For Discriminatedmentioning

confidence: 99%

“…Previous support for a role of serial circuitry that connects the VMS and DLS comes from a study that combined lesioning of the VMS on one side of the brain and antagonism of dopamine receptors in the contralateral DLS, thereby functionally disconnecting serial interactions between these striatal domains on both sides of the brain (23). Although either manipulation on its own was without effect, the combined procedures selectively decreased cocaine seeking in extensively trained rats but not in rats that had undergone only moderate training (23).…”

Section: Dopamine Signaling In the Sensorimotor Striatum Emerges Beforementioning

confidence: 99%

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Hierarchical recruitment of phasic dopamine signaling in the striatum during the progression of cocaine use

Willuhn

Burgeno

Everitt

et al. 2012

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

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233

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Drug addiction is a neuropsychiatric disorder that marks the end stage of a progression beginning with recreational drug taking but culminating in habitual and compulsive drug use. This progression is considered to reflect transitions among multiple neural loci. Dopamine neurotransmission in the ventromedial striatum (VMS) is pivotal in the control of initial drug use, but emerging evidence indicates that once drug use is well established, its control is dominated by the dorsolateral striatum (DLS). In the current work, we conducted longitudinal neurochemical recordings to ascertain the spatiotemporal profile of striatal dopamine release and to investigate how it changes during the period from initial to established drug use. Dopamine release was detected using fast-scan cyclic voltammetry simultaneously in the VMS and DLS of rats bearing indwelling i.v. catheters over the course of 3 wk of cocaine self-administration. We found that phasic dopamine release in DLS emerged progressively during drug taking over the course of weeks, a period during which VMS dopamine signaling declined. This emergent dopamine signaling in the DLS mediated discriminated behavior to obtain drug but did not promote escalated or compulsive drug use. We also demonstrate that this recruitment of dopamine signaling in the DLS is dependent on antecedent activity in VMS circuitry. Thus, the current findings identify a striatal hierarchy that is instantiated during the expression of established responses to obtain cocaine. D rug use often begins as a recreational behavior driven by the rewarding properties of the abused drug. However, addiction is characterized by habitual and compulsive drug use in which other factors, such as withdrawal symptoms, stress, and drug-associated conditioned stimuli (CS), also contribute to the motivation to consume drugs, and drug taking becomes increasingly prioritized over other behaviors (1). A wealth of evidence shows that the mesolimbic dopamine projection from the ventral tegmental area to the ventromedial striatum (VMS) is central to drug reinforcement (2). The ambient concentration of dopamine in the VMS is increased when animals self-administer drugs of abuse, including cocaine (3), and animals maintain this elevated dopamine level by regulating their rate of responding for drug (4). In addition, with repeated pairing of environmental stimuli with the drug, these CS also gain the propensity to elicit changes in dopamine concentration in the VMS (5-8); and even though these phasic neurochemical responses last only a few seconds, they are capable of controlling drug-seeking and -taking behavior (5). Together, these results implicate dopamine release in the VMS as a critical substrate in the control of drug use (2, 3, 9).However, the progression of drug taking beyond recreational use is thought to reflect the engagement of different psychological processes mediated within several neural loci (10, 11), with a particular emphasis on the incorporation of the sensorimotor (dorsolateral) striatum (DLS) in the c...

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Section: Dopamine Signaling In the Sensorimotor Striatum Emerges Beforesupporting

confidence: 79%

Section: Dopamine Receptors In the Dls Are Necessary For Discriminatedmentioning

confidence: 99%

Section: Dopamine Signaling In the Sensorimotor Striatum Emerges Beforementioning

confidence: 99%

See 1 more Smart Citation

Hierarchical recruitment of phasic dopamine signaling in the striatum during the progression of cocaine use

Willuhn

Burgeno

Everitt

et al. 2012

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

Self Cite

233

210

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“…The striatum has long been implicated in learning (Atallah, Lopez-Paniagua, Rudy, & O'Reilly, 2007), and connectivity between the ventral and dorsal striatum is essential for learning (Belin & Everitt, 2008). In a study by den Ouden et al (2009), the putamen (and dorsolateral prefrontal cortex) have been implicated in the acquisition of cue-target learning over time as modeled by a Rescorla-Wagner model, and shown to be sensitive to unexpected outcomes even when those are task irrelevant and learned incidentally, as is the case in the current study.…”

Section: A Common System For Category and Location Regularitysupporting

confidence: 49%

Predictability of what or where reduces brain activity, but a bottleneck occurs when both are predictable

Davis

Hasson

2018

NeuroImage

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Detecting regularities in the sensory environment licenses predictions that enable adaptive behaviour. However, it is unclear whether predictions about object category, location, or both dimensions are mediated by overlapping systems, and relatedly, whether constructing predictions about both category and location is associated with processing bottlenecks. To examine this issue, in an fMRI study, we presented participants with image-series in which non-deterministic transition probabilities enabled predictions about either the location of the next image, its semantic category, both dimensions, or neither (the latter forming a "no-regularity" random baseline condition). Speaking to a common system, all three predictable conditions resulted in reduced BOLD activity in four clusters: left rostral anterior cingulate cortex; bilateral putamen, caudate and thalamus; right precentral gyrus, and left visual cortex. Pointing to a processing bottleneck, in some regions, a significant interaction between the two factors was found whereby category-predictable series were associated with lower activity -but only when location regularity was absent. Finally, category regularity decreased activation in areas of the ventral visual stream and semantic areas of lateral temporal cortex, and location regularity decreased activation in a dorsal fronto-parietal cluster, long implicated in the endogenous control of spatial attention. Our findings confirm and expand a role for dACC/dmPFC and striatum in monitoring or responding to uncertainty in the environment and point to a limited capacity bottleneck when multiple predictions are concurrently licensed.

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“…It has been suggested that after extended training, habits become deeply engrained by shifting further dorsally in the corticostriatal loops (Belin and Everitt, 2008;Willuhn et al, 2012). Using cyclic voltammetry and a behavioural paradigm similar to sign-tracking paradigm, Clark et al (2013) examined changes in dopamine release in the nucleus accumbens core during the acquisition and maintenance of a Pavlovian conditioned approach response (i.e.…”

Section: Shifts Towards Model-free Learning In Addictionmentioning

confidence: 99%

The role of learning-related dopamine signals in addiction vulnerability

Huys

Tobler

Hasler

et al. 2014

Progress in Brain Research

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Psychostimulants such as methylphenidate (MPH) and antidepressants such as fluoxetine (FLX) are widely used in the treatment of various mental disorders or as cognitive enhancers. These medications are often combined, for example, to treat comorbid disorders. There is a considerable body of evidence from animal models indicating that individually these psychotropic medications can have detrimental effects on the brain and behavior, especially when given during sensitive periods of brain development. However, almost no studies investigate possible interactions between these drugs. This is surprising given that their combined neurochemical effects (enhanced dopamine and serotonin neurotransmission) mimic some effects of illicit drugs such as cocaine and amphetamine. Here, we summarize recent studies in juvenile rats on the molecular effects in the mid-and forebrain and associated behavioral changes, after such combination treatments. Our findings indicate that these combined MPH + FLX treatments can produce similar molecular changes as seen after cocaine exposure while inducing behavioral changes indicative of dysregulated mood and motivation, effects that often endure into adulthood. Tables: 2 References: 254 ABSTRACT Dopaminergic signals play a mathematically precise role in reward-related learning, and variations in dopaminergic signalling have been implicated in vulnerability to addiction. Here, we provide a detailed overview of the relationship between theoretical, mathematical and experimental accounts of phasic dopamine signalling, with implications for the role of learning-related dopamine signalling in addiction and related disorders. We describe the theoretical and behavioural characteristics of model-free learning based on errors in the prediction of reward, including step-by-step explanations of the underlying equations. We then use recent insights from an animal model that highlights individual variation in learning during a Pavlovian conditioning paradigm to describe overlapping aspects of incentive salience attribution and model-free learning. We argue that this provides a computationally coherent account of some features of addiction. CONTENTS

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Cocaine Seeking Habits Depend upon Dopamine-Dependent Serial Connectivity Linking the Ventral with the Dorsal Striatum

Cited by 645 publications

References 60 publications

Hierarchical recruitment of phasic dopamine signaling in the striatum during the progression of cocaine use

Hierarchical recruitment of phasic dopamine signaling in the striatum during the progression of cocaine use

Predictability of what or where reduces brain activity, but a bottleneck occurs when both are predictable

The role of learning-related dopamine signals in addiction vulnerability

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