Anticipation of monetary reward in amygdala, insula, caudate are predictors of pleasure sensitivity to d-Amphetamine administration

Langenecker, Scott A.; Kling, Leah R.; Crane, Natania A.; Gorka, Stephanie M.; Nusslock, Robin; Damme, Katherine S.F.; Weafer, Jessica; Wit, Harriet de; Phan, K. Luan

doi:10.1016/j.drugalcdep.2019.107725

Cited by 16 publications

(10 citation statements)

References 87 publications

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“…Consistent with this hypothesis, we recently showed that greater activation in mesolimbic reward regions to monetary reward anticipation in a drug-free state was associated with greater subjective rewarding effects of acute d-amphetamine [51,52]. Using a design similar to the one described here, healthy young adults participated in behavioral sessions in which they received amphetamine and placebo, followed by a drug-free imaging session to assess neural response to monetary reward.…”

Section: Introductionsupporting

confidence: 62%

Striatal activation to monetary reward is associated with alcohol reward sensitivity

Radoman

Crane

Gorka

et al. 2020

Neuropsychopharmacol.

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One well-known phenotypic risk factor for the development of alcohol use disorder is sensitivity to the rewarding effects of alcohol.In the present study, we examined whether individuals who are sensitive to alcohol reward are also sensitive to nondrug rewards, thereby reflecting a broader individual difference risk factor. Specifically, we tested the hypothesis that subjective response to acute rewarding effects of alcohol would be related to neural activation during monetary reward receipt relative to loss (in the absence of alcohol). Community-recruited healthy young social drinkers (N = 58) completed four laboratory sessions in which they received alcohol (0.8 g/kg) and placebo in alternating order under double-blind conditions, providing self-report measures of subjective response to alcohol at regular intervals. At a separate visit 1-3 weeks later, they completed a reward-guessing game, the 'Doors' task, during fMRI in a drug-free state. Participants who reported greater motivation (i.e., wanting) to consume more alcohol after a single moderate dose of alcohol also exhibited greater neural activation in the bilateral ventral caudate and the nucleus accumbens during reward receipt relative to loss. Striatal activation was not related to other subjective ratings including alcohol-induced sedation, stimulation, or pleasure (i.e., feeling, liking). Our study is the first to show that measures of alcohol reward are related to neural indices of monetary reward in humans. These results support growing evidence that individual differences in responses to drug and nondrug reward are linked and together form a risk profile for drug use or abuse, particularly in young adults.

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Section: Introductionsupporting

confidence: 62%

Striatal activation to monetary reward is associated with alcohol reward sensitivity

Radoman

Crane

Gorka

et al. 2020

Neuropsychopharmacol.

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“…43 Furthermore, activation of insula and striatum during reward-based tasks are associated with liking of amphetamine. 44 Here, we show that DA activity is altered in these regions following amphetamine intake, with the exception for medial temporal lobe. The absence of occupancy change in medial temporal lobe was partly surprising given significant amphetamine-induced DA level elevations in past microdialysis work.…”

Section: Discussionmentioning

confidence: 55%

Amphetamine-induced dopamine release in rat: Whole-brain spatiotemporal analysis with [¹¹C]raclopride and positron emission tomography

Johansson,

Ericsson,

Axelsson

et al. 2023

J Cereb Blood Flow Metab

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Whole-brain mapping of drug effects are needed to understand the neural underpinnings of drug-related behaviors. Amphetamine administration is associated with robust increases in striatal dopamine (DA) release. Dopaminergic terminals are, however, present across several associative brain regions, which may contribute to behavioral effects of amphetamine. Yet the assessment of DA release has been restricted to a few brain regions of interest. The present work employed positron emission tomography (PET) with [11C]raclopride to investigate regional and temporal characteristics of amphetamine-induced DA release across twenty sessions in adult female Sprague Dawley rats. Amphetamine was injected intravenously (2 mg/kg) to cause displacement of [11C]raclopride binding from DA D2-like receptors, assessed using temporally sensitive pharmacokinetic PET model (lp-ntPET). We show amphetamine-induced [11C]raclopride displacement in the basal ganglia, and no changes following saline injections. Peak occupancy was highest in nucleus accumbens, followed by caudate-putamen and globus pallidus. Importantly, significant amphetamine-induced displacement was also observed in several extrastriatal regions, and specifically in thalamus, insula, orbitofrontal cortex, and secondary somatosensory area. For these, peak occupancy occurred later and was lower as compared to the striatum. Collectively, these findings demonstrate distinct amphetamine-induced DA responses across the brain, and that [11C]raclopride-PET can be employed to detect such spatiotemporal differences.

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“…The MeA also showed significant resting state connectivity throughout the insula. Nearly all subregions of the amygdala are reciprocally connected with the insula (Mufson et al, 1981 ) and amygdala-insula connections are thought to govern disgust, appetite, reward, and satiety (Sarinopoulos et al, 2006 ; Boutelle et al, 2015 ; Langenecker et al, 2020 ). Further research is needed to understand whether extensive connectivity between the MeA and the insula represents an olfactory function.…”

Section: Discussionmentioning

confidence: 99%

“…The resting state connectivity map of the CoA included the caudate and substantia nigra, both of which have been shown to exhibit connectivity with the amygdala, as components of a well-studied limbic anticipatory-reward circuit (Lee et al, 2006 ; Langenecker et al, 2020 ). The CoA also showed significant resting state connectivity with the periaqueductal gray (PAG) area, which is involved in respiratory control and motivated behaviors (Motta et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions

Noto

Zhou

Yang

et al. 2021

Front. Syst. Neurosci.

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Three subregions of the amygdala receive monosynaptic projections from the olfactory bulb, making them part of the primary olfactory cortex. These primary olfactory areas are located at the anterior-medial aspect of the amygdala and include the medial amygdala (MeA), cortical amygdala (CoA), and the periamygdaloid complex (PAC). The vast majority of research on the amygdala has focused on the larger basolateral and basomedial subregions, which are known to be involved in implicit learning, threat responses, and emotion. Fewer studies have focused on the MeA, CoA, and PAC, with most conducted in rodents. Therefore, our understanding of the functions of these amygdala subregions is limited, particularly in humans. Here, we first conducted a review of existing literature on the MeA, CoA, and PAC. We then used resting-state fMRI and unbiased k-means clustering techniques to show that the anatomical boundaries of human MeA, CoA, and PAC accurately parcellate based on their whole-brain resting connectivity patterns alone, suggesting that their functional networks are distinct, relative both to each other and to the amygdala subregions that do not receive input from the olfactory bulb. Finally, considering that distinct functional networks are suggestive of distinct functions, we examined the whole-brain resting network of each subregion and speculated on potential roles that each region may play in olfactory processing. Based on these analyses, we speculate that the MeA could potentially be involved in the generation of rapid motor responses to olfactory stimuli (including fight/flight), particularly in approach/avoid contexts. The CoA could potentially be involved in olfactory-related reward processing, including learning and memory of approach/avoid responses. The PAC could potentially be involved in the multisensory integration of olfactory information with other sensory systems. These speculations can be used to form the basis of future studies aimed at clarifying the olfactory functions of these under-studied primary olfactory areas.

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Anticipation of monetary reward in amygdala, insula, caudate are predictors of pleasure sensitivity to d-Amphetamine administration

Abstract: Background-Drug addiction and dependence continue as an unresolved source of morbidity and mortality. Two approaches to identifying risk for abuse and addiction are psychopharmacological challenge studies and neuroimaging experiments. The present study

Cited by 16 publications

References 87 publications

Striatal activation to monetary reward is associated with alcohol reward sensitivity

Striatal activation to monetary reward is associated with alcohol reward sensitivity

Amphetamine-induced dopamine release in rat: Whole-brain spatiotemporal analysis with [¹¹C]raclopride and positron emission tomography

Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions

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Anticipation of monetary reward in amygdala, insula, caudate are predictors of pleasure sensitivity to d-Amphetamine administration

Abstract: Background-Drug addiction and dependence continue as an unresolved source of morbidity and mortality. Two approaches to identifying risk for abuse and addiction are psychopharmacological challenge studies and neuroimaging experiments. The present study

Cited by 16 publications

References 87 publications

Striatal activation to monetary reward is associated with alcohol reward sensitivity

Striatal activation to monetary reward is associated with alcohol reward sensitivity

Amphetamine-induced dopamine release in rat: Whole-brain spatiotemporal analysis with [11C]raclopride and positron emission tomography

Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions

Contact Info

Product

Resources

About

Amphetamine-induced dopamine release in rat: Whole-brain spatiotemporal analysis with [¹¹C]raclopride and positron emission tomography