The Anterior Insular Cortex→Central Amygdala Glutamatergic Pathway Is Critical to Relapse after Contingency Management

Vènniro, Marco; Caprioli, Daniele; Zhang, Michelle; Whitaker, Leslie R.; Zhang, Shiliang; Warren, Brandon L.; Cifani, Carlo; Marchant, Nathan J.; Yizhar, Ofer; Bossert, Jennifer M.; Chiamulera, Cristiano; Morales, Marisela; Shaham, Yavin

doi:10.1016/j.neuron.2017.09.024

Cited by 140 publications

(174 citation statements)

References 94 publications

(158 reference statements)

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“…There was a near‐significant decrease in BLA Arc immunoreactivity after guanfacine, which is consistent with previous research using in vivo electrophysiology and clonidine in the BLA . The CeA has a well‐established role in stress‐induced behaviors, and the CeL but not the CeM mediates relapse to methamphetamine self‐administration . Guanfacine increased CeL Arc immunoreactivity (Figure C,D), as seen previously, but nicotine‐treated groups showed decreased CeL activity overall.…”

Section: Discussionsupporting

confidence: 76%

Variability in nicotine conditioned place preference and stress‐induced reinstatement in mice: Effects of sex, initial chamber preference, and guanfacine

Lee

Calarco

McKee

et al. 2019

Genes Brain and Behavior

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Relapse to smoking occurs at higher rates in women compared with men, especially when triggered by stress. Studies suggest that sex‐specific interactions between nicotine reward and stress contribute to these sex differences. Accordingly, novel treatment options targeting stress pathways, such as guanfacine, an α2‐adrenergic receptor agonist, may provide sex‐sensitive therapeutic effects. Preclinical studies are critical for elucidating neurobiological mechanisms of stress‐induced relapse and potential therapies, but rodent models of nicotine addiction are often hindered by large behavioral variability. In this study, we used nicotine conditioned place preference to investigate stress‐induced reinstatement of nicotine preference in male and female mice, and the effects of guanfacine on this behavior. Our results showed that overall, nicotine induced significant place preference acquisition and swim stress‐induced reinstatement in both male and female mice, but with different nicotine dose‐response patterns. In addition, we explored the variability in nicotine‐dependent behaviors with median split analyses and found that initial chamber preference in each sex differentially accounted for variability in stress‐induced reinstatement. In groups that showed significant stress‐induced reinstatement, pretreatment with guanfacine attenuated this behavior. Finally, we evaluated neuronal activation by Arc immunoreactivity in the infralimbic cortex, prelimbic cortex, anterior insula, basolateral amygdala, lateral central amygdala and nucleus accumbens core and shell. Guanfacine induced sex‐dependent changes in Arc immunoreactivity in the infralimbic cortex and anterior insula. This study demonstrates sex‐dependent relationships between initial chamber preference and stress‐induced reinstatement of nicotine conditioned place preference, and the effects of guanfacine on both behavior and neurobiological mechanisms.

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Section: Discussionsupporting

confidence: 76%

Variability in nicotine conditioned place preference and stress‐induced reinstatement in mice: Effects of sex, initial chamber preference, and guanfacine

Lee

Calarco

McKee

et al. 2019

Genes Brain and Behavior

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Section: Viral Methods For Chemogenetic Receptor Expressionmentioning

confidence: 97%

“…In addition, intracranial cannulas are implanted above the projection target region. To date, several studies have used local infusions of CNO into the projection target region to cause selective manipulation of only the DREADD-expressing terminals in the target region (Lichtenberg et al, 2017;Mahler et al, 2014;McGlinchey and Aston-Jones, 2017;Stachniak et al, 2014;Venniro et al, 2017). For example, Ge et al (2017) used this approach to show that inactivation of entorhinal cortex terminals in the dorsal dentate gyrus significantly decreased contextinduced reinstatement of heroin seeking.…”

Section: Circuit-specific Uses Of Chemogeneticsmentioning

confidence: 99%

The use of chemogenetics in behavioural neuroscience: receptor variants, targeting approaches and caveats

Campbell

Marchant

2018

British J Pharmacology

101

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The last decade has seen major advances in neuroscience tools allowing us to selectively modulate cellular pathways in freely moving animals. Chemogenetic approaches such as designer receptors exclusively activated by designer drugs (DREADDs) permit the remote control of neuronal function by systemic drug administration. These approaches have dramatically advanced our understanding of the neural control of behaviour. Here, we review the different techniques and genetic approaches available for the restriction of chemogenetic receptors to defined neuronal populations. We highlight the use of a dual virus approach to target specific circuitries and the effectiveness of different routes of administration of designer drugs. Finally, we discuss the potential caveats associated with DREADDs including off-target effects of designer drugs, the effects of chronic chemogenetic receptor activation and the issue of collateral projections associated with DREADD activation and inhibition. AbbreviationsAAVs, adeno-associated viral vectors; BBB, blood-brain barrier; CAMKII, calmodulin-dependent protein kinase II; CAVs, canine adenoviruses; CNO, clozapine N-oxide; DREADDs, designer receptors exclusively activated by designer drugs; hM3D, human M 3 muscarinic DREADD; hM4D, human M 4 muscarinic DREADD; HSV, herpes simplex viral; hSyn, human synapsin; KORD, κ-opioid-based receptor designer receptor exclusively activated by designer drugs; LGICs, ligand-gated ion channels; NAc, nucleus accumbens; RASSL, receptor activated solely by a synthetic ligand; SalB, salvinorin B; VTA, ventral tegmental area IntroductionDuring the last decade, there has been a revolution in neuroscience techniques that have resulted in increasingly precise methods to manipulate neural systems in awake, behaving animals. Understanding the relationship between brain function and behaviour is critical for the advancement of both neuroscience research and targeted medication development. Chemogenetics refers to the technique that allows for the reversible remote control of cell populations and neural circuitry via systemic injection or microinfusion of an activating ligand (Alexander et al., 2009;Armbruster et al., 2007). The chemogenetic technique uses engineered receptors and biologically inert ligands to achieve this aim. Unlike optogenetics, which has the ability to control cells and neural circuitry with light, the use of designer drugs makes chemogenetics simple to use, removing the need for optical fibre probes and tethers. While the temporal resolution of chemogenetics is lower than optogenetics, this relatively non-invasive technique is still effective for functional mapping, cell-type-specific manipulations and multiplexed control of neurons.In this review, we will evaluate the different strategies that have been used to restrict chemogenetic receptors to defined neuronal populations. We will also highlight the use of a dual virus approach at targeting projection neurons and the effectiveness of different routes of administration of designer drugs. Fin...

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“…Beyond its role in fear‐related behaviours, the amygdala has been shown to be involved in drug addiction (Makris et al., ; Wrase et al., ; Xie et al., ; Zill et al., ). Most notably, the central amygdala (CeA) has been reported as crucial for the incubation of craving for drugs such as nicotine, cocaine, morphine and methamphetamine (Funk et al., ; Li, Zeric, Kambhampati, Bossert, & Shaham, ; Li et al., ; Lu, Uejima, Gray, Bossert, & Shaham, ; Lu et al., ; Venniro et al., ). In recent studies, we have also shown that the CeA is involved in the development of compulsive choice of food and drug reward (Robinson, Warlow, & Berridge, ; Warlow, Robinson, & Berridge, ).…”

Section: Introductionmentioning

confidence: 99%

Optogenetic activation of the central amygdala generates addiction‐like preference for reward

Tom

Ahuja

Maniates

et al. 2018

Eur J of Neuroscience

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Drug and behavioural addictions are characterized by an intense and focused pursuit of a single reward above all others. Pursuit of the addictive reward is often compulsively sought despite adverse consequences and better alternative outcomes. Here, we explored the ability of the central amygdala (CeA) to powerfully bias choice, causing specific rewards to be almost compulsively preferred. Rats were trained on an operant choice task in which they could choose to respond on either of the two levers to receive a sucrose reward, one of which was paired with optogenetic stimulation of the CeA using channelrhodopsin-2 (ChR2). Rats developed an almost exclusive preference for the laser-paired reward over the otherwise equal unpaired reward. We found that this preference for stimulation-paired reward persists even when a much larger sucrose reward is offered as an alternative (contingency management) or when this preferred reward is paired with adverse consequences such as progressively larger electric foot shock, time delays or effort requirements. We also report that when challenged with foot shock, a small proportion of these animals (≈20%) retained an exclusive laser-paired reward preference, whereas others began to seek the alternate reward when the shock reached high levels. Lastly, we confirmed that optogenetic CeA stimulation was not independently rewarding if delivered in the absence of a paired sucrose reward. These results suggest a role for the CeA in focusing motivation and desire to excessive levels, generating addiction-like behaviour that persists in the face of more rewarding alternatives and adverse consequences.

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The Anterior Insular Cortex→Central Amygdala Glutamatergic Pathway Is Critical to Relapse after Contingency Management

Cited by 140 publications

References 94 publications

Variability in nicotine conditioned place preference and stress‐induced reinstatement in mice: Effects of sex, initial chamber preference, and guanfacine

Variability in nicotine conditioned place preference and stress‐induced reinstatement in mice: Effects of sex, initial chamber preference, and guanfacine

The use of chemogenetics in behavioural neuroscience: receptor variants, targeting approaches and caveats

Optogenetic activation of the central amygdala generates addiction‐like preference for reward

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