δ-Opioid and dopaminergic processes in accumbens shell modulate the cholinergic control of predictive learning and choice

Laurent, Vincent, Bertran-Gonzalez, Jesus, Chieng, Billy C. and Balleine B.W. (2014) δ-Opioid and dopaminergic processes in accumbens shell modulate the cholinergic control of predictive learning and choice. Journal of Neuroscience, 34 4: 1358-1369. doi:10.1523/JNEUROSCI.4592-13.2014

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Author Laurent, Vincent
Bertran-Gonzalez, Jesus
Chieng, Billy C.
Balleine B.W.
Title δ-Opioid and dopaminergic processes in accumbens shell modulate the cholinergic control of predictive learning and choice
Journal name Journal of Neuroscience   Check publisher's open access policy
ISSN 0270-6474
1529-2401
Publication date 2014-01-01
Sub-type Article (original research)
DOI 10.1523/JNEUROSCI.4592-13.2014
Open Access Status File (Publisher version)
Volume 34
Issue 4
Start page 1358
End page 1369
Total pages 12
Place of publication Washington, DC, United States
Publisher Society for Neuroscience
Collection year 2015
Language eng
Abstract Decision-making depends on the ability to extract predictive information from the environment to guide future actions. Outcome-specific Pavlovian-instrumental transfer (PIT) provides an animal model of this process in which a stimulus predicting a particular outcome biases choice toward actions earning that outcome. Recent evidence suggests that cellular adaptations of δ-opioid receptors (DORs) on cholinergic interneurons (CINs) in the nucleus accumbens shell (NAc-S) are necessary for PIT. Here we found that modulation of DORs in CINs critically influences D1-receptor (D1R)-expressing projection neurons in the NAc-S to promote PIT. First, we assessed PIT-induced changes in signaling processes in dopamine D1- and D2-receptor-expressing neurons using drd2-eGFP mice, and found that PIT-related signaling was restricted to non-D2R-eGFP-expressing neurons, suggesting major involvement of D1R-neurons. Next we confirmed the role of D1Rs pharmacologically: the D1R antagonist SCH-23390, but not the D2R antagonist raclopride, infused into the NAc-S abolished PIT in rats, an effect that depended on DOR activity. Moreover, asymmetrical infusion of SCH-23390 and the DOR antagonist naltrindole into the NAc-S also abolished PIT. DOR agonists were found to sensitize the firing responses of CINs in brain slices prepared immediately after the PIT test. We confirmed the opioid-acetylcholinergic influence over D1R-neurons by selectively blocking muscarinic M4 receptors in the NAc-S, which tightly regulate the activity of D1Rs, a treatment that rescued the deficit in PIT induced by naltrindole. We describe a model of NAc-S function in which DORs modulate CINs to influence both D1R-neurons and stimulus-guided choice between goal-directed actions.
Keyword δ-opioid receptor
Choice
Dopamine receptor
Goal-directed action
Muscarinic acetylcholine receptor M4
Nucleus accumbens shell
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Queensland Brain Institute Publications
Official 2015 Collection
 
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Citation counts: TR Web of Science Citation Count  Cited 16 times in Thomson Reuters Web of Science Article | Citations
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