Activating Corticotropin-Releasing Factor Systems in the Nucleus Accumbens, Amygdala, and Bed Nucleus of Stria Terminalis: Incentive Motivation or Aversive Motivation?

Baumgartner, Hannah; Schulkin, Jay; Berridge, Kent

doi:10.1016/j.biopsych.2021.01.007

Cited by 47 publications

(45 citation statements)

References 67 publications

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“…However, despite ample evidence that CRF systems can contribute to negative distress, other findings suggest that CRF-containing neurons in CeA and nucleus accumbens (NAc) alternatively have positively-valenced or incentive-mediated psychological routes to cause intense pursuit and consumption of rewards [ 14 – 18 ]. For example, optogenetic stimulation of CRF-containing neurons in CeA and NAc of C rh -Cre+ rats recruited reward-related mesocorticolimbic circuitry to increase incentive motivation for sucrose reward, and narrowly-focused pursuit on laser-paired sucrose [ 19 ]. Demonstrating positive-valence, most of those rats actively worked for laser to self-stimulate their CRF-containing neurons in CeA and NAc.…”

Section: Introductionmentioning

confidence: 99%

“…Such observations indicate that CRF neural systems in CeA and NAc may increase incentive motivation for sucrose reward via a positively-valenced process [ 19 ]. Incentive salience or ‘wanting’ is a specific mesolimbic-mediated motivational process that attributes positive incentive value to neural representations of rewards and their cues.…”

Section: Introductionmentioning

confidence: 99%

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Corticotropin releasing factor (CRF) systems: Promoting cocaine pursuit without distress via incentive motivation

et al. 2022

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Corticotropin releasing factor (CRF) systems in limbic structures are posited to mediate stress-induced relapse in addiction, traditionally by generating distress states that spur drug consumption as attempts at hedonic self-medication. Yet evidence suggests that activating CRF-expressing neurons in the central amygdala (CeA) or nucleus accumbens (NAc) can magnify incentive motivation in absence of distress, at least for sucrose rewards. However, traditional CRF hypotheses in addiction neuroscience are primarily directed toward drug rewards. The question remains open whether CRF systems can similarly act via incentive motivation mechanisms to promote pursuit of drug rewards, such as cocaine. Here we tested whether optogenetic excitation of CRF-containing neurons in either NAc medial shell, lateral CeA, or dorsolateral BNST of transgenic Crh-Cre+ rats would spur preference and pursuit of a particular laser-paired cocaine reward over an alternative cocaine reward, and whether excitation served as a positively-valenced incentive itself, through laser self-stimulation tests. We report that excitation of CRF-containing neurons in either NAc or CeA recruited mesocorticolimbic circuitry to amplify incentive motivation to pursue the laser-paired cocaine: focusing preference on the laser-paired cocaine reward in a two-choice task, and spurred pursuit as doubled breakpoint in a progressive ratio task. Crucially indicating positive-valence, excitation of CRF neurons in NAc and CeA also was actively sought after by most rats in self-stimulation tasks. Conversely, CRF neuronal activation in BNST was never self-stimulated, but failed to enhance cocaine consumption. Collectively, we find that NAc and CeA CRF-containing neurons can amplify pursuit and consumption of cocaine by positively-valenced incentive mechanisms, without any aversive distress.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Corticotropin releasing factor (CRF) systems: Promoting cocaine pursuit without distress via incentive motivation

et al. 2022

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“…The Pu seems to participate in motor learning ( Liebrand et al, 2020 ), auditory responses ( Salisbury et al, 2021 ), cocaine addiction ( Ersche et al, 2021 ), and psychiatric disorders ( Kolomeets and Uranova, 2020 ). In addition, the Acb is involved in motor control ( Sawada et al, 2015 ), reward processing ( Muench et al, 2018 ), motivation ( Baumgartner et al, 2021 ), addiction ( Crofton et al, 2021 ), mental disorders ( Terrillion et al, 2017 ), and social defeat stress ( Yin et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Whole-Brain Afferent Inputs to the Caudate Nucleus, Putamen, and Accumbens Nucleus in the Tree Shrew Striatum

Shu

et al. 2021

Front. Neuroanat.

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Day-active tree shrews have a well-developed internal capsule (ic) that clearly separates the caudate nucleus (Cd) and putamen (Pu). The striatum consists of the Cd, ic, Pu, and accumbens nucleus (Acb). Here, we characterized the cytoarchitecture of the striatum and the whole-brain inputs to the Cd, Pu, and Acb in tree shrews by using immunohistochemistry and the retrograde tracer Fluoro-Gold (FG). Our data show the distribution patterns of parvalbumin (PV), nitric oxide synthase (NOS), calretinin (CR), and tyrosine hydroxylase (TH) immunoreactivity in the striatum of tree shrews, which were different from those observed in rats. The Cd and Pu mainly received inputs from the thalamus, motor cortex, somatosensory cortex, subthalamic nucleus, substantia nigra, and other cortical and subcortical regions, whereas the Acb primarily received inputs from the anterior olfactory nucleus, claustrum, infralimbic cortex, thalamus, raphe nucleus, parabrachial nucleus, ventral tegmental area, and so on. The Cd, Pu, and Acb received inputs from different neuronal populations in the ipsilateral (60, 67, and 63 brain regions, respectively) and contralateral (23, 20, and 36 brain regions, respectively) brain hemispheres. Overall, we demonstrate that there are species differences between tree shrews and rats in the density of PV, NOS, CR, and TH immunoreactivity in the striatum. Additionally, we mapped for the first time the distribution of whole-brain input neurons projecting to the striatum of tree shrews with FG injected into the Cd, Pu, and Acb. The similarities and differences in their brain-wide input patterns may provide new insights into the diverse functions of the striatal subregions.

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“…Corticotropin-releasing factor signaling via CRF receptor-1 (CRF1R) and CRF receptor-2 (CRF2R), and is a preferential agonist for CRF1R over CRF2R. Corticotropin-releasing factor receptors widely signal throughout the brain, such as the ventral tegmental area (VTA), NAc, amygdala, and bed nucleus of the stria terminalis ( Baumgartner et al, 2021 ). It was reported that the CRF-induced increase in the activity of dopamine (DA) neurons in the VTA might enhance release in the NAc, which potentiates drug-seeking behaviors and the response to reward ( Wanat et al, 2008 ).…”

Section: Introductionmentioning

confidence: 99%

The Antagonism of Corticotropin-Releasing Factor Receptor-1 in Brain Suppress Stress-Induced Propofol Self-Administration in Rats

Dong

Zhang

Xiang

et al. 2021

Front. Behav. Neurosci.

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Propofol addiction has been detected in humans and rats, which may be facilitated by stress. Corticotropin-releasing factor acts through the corticotropin-releasing factor (CRF) receptor-1 (CRF1R) and CRF2 receptor-2 (CRF2R) and is a crucial candidate target for the interaction between stress and drug abuse, but its role on propofol addiction remains unknown. Tail clip stressful stimulation was performed in rats to test the stress on the establishment of the propofol self-administration behavioral model. Thereafter, the rats were pretreated before the testing session at the bilateral lateral ventricle with one of the doses of antalarmin (CRF1R antagonist, 100–500 ng/site), antisauvagine 30 (CRF2R antagonist, 100–500 ng/site), and RU486 (glucocorticoid receptor antagonist, 100–500 ng/site) or vehicle. The dopamine D1 receptor (D1R) in the nucleus accumbens (NAc) was detected to explore the underlying molecular mechanism. The sucrose self-administration establishment and maintenance, and locomotor activities were also examined to determine the specificity. We found that the establishment of propofol self-administration was promoted in the tail clip treated group (the stress group), which was inhibited by antalarmin at the dose of 100–500 ng/site but was not by antisauvagine 30 or RU486. Accordingly, the expression of D1R in the NAc was attenuated by antalarmin, dose-dependently. Moreover, pretreatments fail to change sucrose self-administration behavior or locomotor activities. This study supports the role of CRF1R in the brain in mediating the central reward processing through D1R in the NAc and provided a possibility that CRF1R antagonist may be a new therapeutic approach for the treatment of propofol addiction.

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Activating Corticotropin-Releasing Factor Systems in the Nucleus Accumbens, Amygdala, and Bed Nucleus of Stria Terminalis: Incentive Motivation or Aversive Motivation?

Cited by 47 publications

References 67 publications

Corticotropin releasing factor (CRF) systems: Promoting cocaine pursuit without distress via incentive motivation

Corticotropin releasing factor (CRF) systems: Promoting cocaine pursuit without distress via incentive motivation

Whole-Brain Afferent Inputs to the Caudate Nucleus, Putamen, and Accumbens Nucleus in the Tree Shrew Striatum

The Antagonism of Corticotropin-Releasing Factor Receptor-1 in Brain Suppress Stress-Induced Propofol Self-Administration in Rats

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