Cooperative CRF and α1 Adrenergic Signaling in the VTA Promotes NMDA Plasticity and Drives Social Stress Enhancement of Cocaine Conditioning

Tovar-Díaz, Jorge; Pomrenze, Matthew B.; Kan, Russell; Pahlavan, Bahram; Morikawa, Hitoshi

doi:10.1016/j.celrep.2018.02.039

Cited by 31 publications

(30 citation statements)

References 84 publications

(115 reference statements)

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“…Brief exposure to acute social defeat stress enhances the conditioned effects of psychostimulants, which may in turn promote the acquisition of self-administration behavior. Compared to non-defeated control animals, both mice and rats that are socially defeated immediately before receiving an injection of cocaine subsequently develop a greater preference for the drug-paired environment during conditioned place preference (CPP) testing ( McLaughlin et al, 2006 ; Montagud-Romero et al, 2015 ; Tovar-Diaz et al, 2018 ). Likewise, exposure to social defeat stress over five consecutive days can double the rate of cocaine self-administration acquisition ( Fig.…”

Section: Animal Models Of Social Stress and Pathological Patterns Of mentioning

confidence: 99%

Social defeat stress and escalation of cocaine and alcohol consumption: Focus on CRF

Newman

Leonard

Arena

et al. 2018

Neurobiology of Stress

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Both the ostensibly aversive effects of unpredictable episodes of social stress and the intensely rewarding effects of drugs of abuse activate the mesocorticolimbic dopamine systems. Significant neuroadaptations in interacting stress and reward neurocircuitry may underlie the striking connection between stress and substance use disorders. In rodent models, recurring intermittent exposure to social defeat stress appears to produce a distinct profile of neuroadaptations that translates most readily to the repercussions of social stress in humans. In the present review, preclinical rodent models of social defeat stress and subsequent alcohol, cocaine or opioid consumption are discussed with regard to: (1) the temporal pattern of social defeat stress, (2) male and female protocols of social stress-escalated drug consumption, and (3) the neuroplastic effects of social stress, which may contribute to escalated drug-taking. Neuroadaptations in corticotropin-releasing factor (CRF) and CRF modulation of monoamines in the ventral tegmental area and the bed nucleus of the stria terminalis are highlighted as potential mechanisms underlying stress-escalated drug consumption. However, the specific mechanisms that drive CRF-mediated increases in dopamine require additional investigation as do the stress-induced neuroadaptations that may contribute to the development of compulsive patterns of drug-taking.

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Section: Animal Models Of Social Stress and Pathological Patterns Of mentioning

confidence: 99%

Social defeat stress and escalation of cocaine and alcohol consumption: Focus on CRF

Newman

Leonard

Arena

et al. 2018

Neurobiology of Stress

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“…), or conversely, by synergizing with corticotrophin‐releasing factor to enhance NMDA‐dependent and IP 3 ‐ and calcium‐mediated plasticity (Tovar‐Díaz et al . ).…”

Section: Discussionmentioning

confidence: 97%

“…The VTA itself is a target for regulation via other systems. This involves glutamate acting via NMDA and a-amino-3hydroxy-5-methylisoxazole-4-propionate receptors, GABAergic interneurons, and inputs that constrain the activity of the VTA, as well as a plethora of modulatory signals including acetylcholine, stress-related signaling encompassing both corticoids and corticoid releasing factor, and finally, noradrenaline (Guiard et al 2008;Lester et al 2008Lester et al , 2010Parker et al 2010;Morikawa and Paladini 2011;Polter and Kauer 2014;Schmidt and Weinshenker 2014;Tovar-D ıaz et al 2018).…”

mentioning

confidence: 99%

Differential regulation of phasic dopamine release in the forebrain by the VTA noradrenergic receptor signaling

Kielbinski

Bernacka

Solecki

2019

Journal of Neurochemistry

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Phasic dopamine (DA) release from the ventral tegmental area (VTA) into forebrain structures is implicated in associative learning and conditional stimulus (CS)‐evoked behavioral responses. Mounting evidence points to noradrenaline signaling in the VTA as an important regulatory input. Accordingly, adrenergic receptor (AR) blockade in the VTA has been shown to modulate CS‐dependent behaviors. Here, we hypothesized that α1‐ and α2‐AR (but not β‐AR) activity preferentially modulates phasic, in contrast to tonic, DA release. In addition, these effects could differ between forebrain targets. We used fast‐scan cyclic voltammetric measurements in rats to assess the effects of intra‐VTA microinfusion of terazosin, a selective α1‐AR antagonist, on electrically evoked phasic DA release in the nucleus accumbens (NAc) core and medial prefrontal cortex (mPFC). Terazosin dose‐dependently attenuated phasic, but not tonic, DA release in the NAc core, but not in the mPFC. Next, we measured the effects of intra‐VTA administration of the α2‐AR selective antagonist RX‐821002 on evoked DA in the NAc core. Similar to the effects of α1‐AR blockade, intra‐VTA α2‐AR blockade with RX‐0821002 strongly and dose‐dependently attenuated phasic, but not tonic, DA release. In contrast, no regulation by RX‐821002 was observed in the mPFC. This effect was sensitive to intra‐VTA blockade of D2 receptors with raclopride. Finally, the β‐AR antagonist propranolol ineffectively modulated DA release in the NAc core. These findings revealed both α1‐ and α2‐ARs in the VTA as selective regulators of phasic DA release. Importantly, we demonstrated that AR blockade modulated mesolimbic, in contrast to mesocortical, DA release in previously unstudied heterogeneity in AR regulation of forebrain phasic DA.

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“…In adverse circumstances, it is adaptive to rapidly and effectively learn which stimuli predict beneficial outcomes. Prior rodent studies have shown that stress enhances the learned preference for a cocaine-associated context 13,14 , though it was unclear if acute stress similarly facilitated learning driven by natural rewards. Here, we addressed this question by utilizing a Pavlovian task in which an auditory CS signaled the upcoming delivery of a food reward.…”

Section: Discussionmentioning

confidence: 99%

Acute stress enhances associative learning via dopamine signaling in the ventral lateral striatum

Stelly

Tritley

Rafati

et al. 2019

Preprint

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AbstractAcute stress transiently increases vigilance, whereby enhancing the detection of salient stimuli. This increased perceptual sensitivity is thought to promote associating rewarding outcomes with relevant cues. The mesolimbic dopamine system is critical for learning cue-reward associations. Dopamine levels in the ventral striatum are elevated following exposure to stress. Together, this suggests the mesolimbic dopamine system could mediate the influence of acute stress on cue-reward learning. To address this possibility, we examined how a single stressful experience influenced learning in an appetitive Pavlovian conditioning task. Male rats underwent an episode of restraint prior to the first conditioning session. This acute stress treatment augmented conditioned responding in subsequent sessions. Voltammetry recordings of mesolimbic dopamine levels demonstrated that acute stress selectively increased reward-evoked dopamine release in the ventral lateral striatum (VLS), but not in the ventral medial striatum (VMS). Antagonizing dopamine receptors in the VLS blocked the stress-induced enhancement of conditioned responding. Collectively, these findings illustrate that stress engages dopamine signaling in the VLS to facilitate appetitive learning.

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Cooperative CRF and α1 Adrenergic Signaling in the VTA Promotes NMDA Plasticity and Drives Social Stress Enhancement of Cocaine Conditioning

Cited by 31 publications

References 84 publications

Social defeat stress and escalation of cocaine and alcohol consumption: Focus on CRF

Social defeat stress and escalation of cocaine and alcohol consumption: Focus on CRF

Differential regulation of phasic dopamine release in the forebrain by the VTA noradrenergic receptor signaling

Acute stress enhances associative learning via dopamine signaling in the ventral lateral striatum

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