Basolateral and central amygdala differentially recruit and maintain dorsolateral striatum-dependent cocaine-seeking habits

Murray, Jennifer E.; Belin, David; Simon, Marine; Giuliano, Chiara; Benoît-Marand, Marianne; Everitt, Barry J.; Belin, David

doi:10.1038/ncomms10088

Cited by 87 publications

(109 citation statements)

References 73 publications

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“…Further, the reduction of associated executive functions, particularly inhibitory control, may result in unwanted habitual behaviours being more difficult to suppress thus further diminishing flexible behavioral control. Amygdala regions may also critically contribute to the expression of goal-directed and habitual behavior, and perhaps the transition from one to the other as shown recently for cocaine (Murray et al, 2015). The basolateral amygdala is important for assigning motivational significance to stimuli based on sensory-specific properties, and damage to this structure impairs sensitivity to outcome devaluation and outcome-specific PIT (Corbit & Balleine, 2005).…”

Section: Mechanismsmentioning

confidence: 84%

Habitual Alcohol Seeking: Neural Bases and Possible Relations to Alcohol Use Disorders

Corbit

Janak

2016

Alcohol Clin Exp Res

100

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Loss of flexible control over alcohol use may contribute to the development of Alcohol Use Disorders. An increased contribution of response habits to alcohol- related behaviors may help explain this loss of control. Focusing on data from outcome devaluation and Pavlovian-instrumental transfer procedures, we review evidence for loss of goal-directed control over alcohol seeking and consumption drawing from both preclinical findings and clinical data where they exist. Over the course of extended alcohol self-administration and exposure, the performance of alcohol-seeking responses becomes less sensitive to reductions in the value of alcohol and more vulnerable to the influences of alcohol-predictive stimuli. These behavioral changes are accompanied by a shift in the corticostriatal circuits that control responding from circuits centered on the dorsomedial to those centered on the dorsolateral striatum. These changes in behavioral and neural control could help explain failures to abstain from alcohol despite intention to do so. Understanding and ultimately ameliorating these changes will aid development of more effective treatment interventions.

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Section: Mechanismsmentioning

confidence: 84%

Habitual Alcohol Seeking: Neural Bases and Possible Relations to Alcohol Use Disorders

Corbit

Janak

2016

Alcohol Clin Exp Res

100

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“…It is striking that modulation of IfL-C activity during consumption was comparable across all conditions, suggesting that processing of contingency and value information is dissociable in IfL-C as a function of response strategy. It should be noted that while loss of IfL-C function is sufficient to occlude habitual reward seeking (Coutureau and Killcross, 2003; Killcross and Coutureau, 2003; Smith et al, 2012), it is by no means the only structure necessary for habits (Yin et al, 2004; Lingawi and Balleine, 2012; Murray et al, 2015). Indeed, using a maze-based task, previous studies demonstrated that coordination between IfL-C and dorsolateral striatum activity is crucial for the development of inflexible behaviors (Smith and Graybiel, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Given the role of IfL-C glutamatergic neurons in the regulation of response strategy (Smith et al, 2012), it is therefore likely that the IfL-C facilitates habitual reward seeking through its action at downstream targets. IfL-C targets multiple structures necessary for the regulation of response strategy selection, including subregions of the amygdala that are differentially involved in the acquisition and expression of habits (Lingawi and Balleine, 2012; Murray et al, 2015). Downstream targets of the IfL-C also include the nucleus accumbens in which IfL-C inputs are required for contingency-mediated behaviors such as appetitive extinction learning (Peters et al, 2008, 2009) and outcome selective Pavlovian-to-instrumental transfer (Keistler et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Habitual Behavior Is Mediated by a Shift in Response-Outcome Encoding by Infralimbic Cortex

Barker

Glen

Linsenbardt

et al. 2017

eNeuro

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The ability to flexibly switch between goal-directed actions and habits is critical for adaptive behavior. The infralimbic prefrontal cortex (IfL-C) has been consistently identified as a crucial structure for the regulation of response strategies. To investigate the role of the IfL-C, the present study employed two validated reinforcement schedules that either promote habits or goal-directed actions in mice. The results reveal that information about action-outcome relationships is differentially encoded in the IfL-C during actions and habits as evidenced by encoding of behavioral outcomes during goal-directed actions that is lost during habits. Optogenetic inhibition of the IfL-C selectively at press during habitual behavior (when firing rates are reduced during unreinforced goal-directed actions) resulted in restoration of sensitivity to change of action-outcome contingency. These results reveal a novel functional mechanism by which IfL-C promotes habitual behavior, and provide insight into strategies for the treatment and prevention of pathological, inflexible behavior common in neuropsychiatric illness.

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“…Following 1 week of habituation to the colony, Lister Hooded rats underwent either both intravenous catheter implantation and bilateral aDLS cannulations (α‐flupenthixol experiment, α‐flu, n = 9) or only the former (N‐acetylcysteine experiment, NAC , n = 14) a week before beginning training. Rats acquired heroin self‐administration under a fixed ratio 1 schedule of reinforcement ( FR 1) under which they were maintained for 10 consecutive daily sessions which were followed by the early stage seeking tests (Murray et al ., , , ). During the early stage seeking tests, rats were challenged to seek heroin over 15 min with CS presented contingently upon each lever press.…”

Section: Methodsmentioning

confidence: 99%

Heroin seeking becomes dependent on dorsal striatal dopaminergic mechanisms and can be decreased by N‐acetylcysteine

Hodebourg

Murray

Fouyssac

et al. 2018

Eur J of Neuroscience

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The alarming increase in heroin overdoses in the USA is a reminder of the need for efficacious and novel treatments for opiate addiction. This may reflect the relatively poor understanding of the neural basis of heroin, as compared to cocaine, seeking behaviour. While cocaine reinforcement depends on the mesolimbic system, well-established cocaine seeking is dependent on dorsolateral striatum (aDLS) dopamine-dependent mechanisms which are disrupted by N-acetylcysteine, through normalisation of corticostriatal glutamate homeostasis. However, it is unknown whether a functional recruitment of aDLS dopamine-dependent control over instrumental responding also occurs for heroin seeking, even though heroin reinforcement does not depend on the mesolimbic dopamine system. Lister Hooded rats acquired heroin self-administration and were subsequently trained to seek heroin daily over prolonged periods of time under the control of drug-paired cues, as measured under a second-order schedule of reinforcement. At different stages of training, that is, early on and when heroin seeking behaviour was well established, we measured the sensitivity of drug-seeking responses to either bilateral aDLS infusions of the dopamine receptor antagonist α-flupenthixol (5, 10 and 15 μg/side) or systemic administration of N-acetylcysteine (30, 60 and 90 mg/kg). The results demonstrate that control over heroin seeking behaviour devolves to aDLS dopamine-dependent mechanisms after extended training. Further aDLS-dependent well-established, cue-controlled heroin seeking was disrupted by N-acetylcysteine. Comparison with previous data on cocaine suggests that the development of drug seeking habits and the alteration of corticostriatal glutamate homeostasis, which is restored by N-acetylcysteine, are quantitatively similar between heroin and cocaine.

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Basolateral and central amygdala differentially recruit and maintain dorsolateral striatum-dependent cocaine-seeking habits

Cited by 87 publications

References 73 publications

Habitual Alcohol Seeking: Neural Bases and Possible Relations to Alcohol Use Disorders

Habitual Alcohol Seeking: Neural Bases and Possible Relations to Alcohol Use Disorders

Habitual Behavior Is Mediated by a Shift in Response-Outcome Encoding by Infralimbic Cortex

Heroin seeking becomes dependent on dorsal striatal dopaminergic mechanisms and can be decreased by N‐acetylcysteine

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