Activation of Basolateral Amygdala to Nucleus Accumbens Projection Neurons Attenuates Chronic Corticosterone-Induced Behavioral Deficits in Male Mice

Dieterich, Andrew; Floeder, Joseph R; Stech, Karina; Lee, Jay; Srivastava, Prachi; Barker, David J.; Samuels, Benjamin Adam

doi:10.3389/fnbeh.2021.643272

Cited by 21 publications

(12 citation statements)

References 78 publications

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“…Further evidence for the role of the BLA-to-NAc circuit comes from recent studies on rescuing behavioral deficits induced by chronic stress (Dieterich et al, 2021;Sun et al, 2021). Collectively, the present results help extend rodent neurobiological findings to humans and indicate that separate patterns of connectivity dissociate CC from standard extinction.…”

Section: Discussionsupporting

confidence: 62%

Rewarded extinction increases amygdalar connectivity and stabilizes long-term memory traces in the vmPFC

Keller

Hennings

Leiker

et al. 2021

Preprint

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Neurobiological evidence in rodents indicates that threat extinction incorporates reward neurocircuitry. Consequently, incorporating reward associations with an extinction memory may be an effective strategy to persistently attenuate threat responses. Moreover, while there is considerable research on the short-term effects of extinction strategies in humans, the long-term effects of extinction are rarely considered. In a within-subjects fMRI study, we compared counterconditioning (a form of rewarded-extinction) to standard extinction, at recent (24 hours) and remote (~1 month) retrieval tests. Relative to standard extinction, counterconditioning diminished 24-hour relapse of arousal and threat expectancy, and reduced activity in brain regions associated with the appraisal and expression of threat (e.g., thalamus, insula, periaqueductal gray). The retrieval of reward-associated extinction memory was accompanied by functional connectivity between the amygdala and the ventral striatum, whereas the retrieval of standard-extinction memories was associated with connectivity between the amygdala and ventromedial prefrontal cortex (vmPFC). One-month later, the retrieval of both standard- and rewarded-extinction was associated with amygdala-vmPFC connectivity. However, only rewarded extinction created a stable memory trace in the vmPFC, identified through overlapping multivariate patterns of fMRI activity from extinction to 24-hour and 1-month retrieval. These findings provide new evidence that reward may generate a more stable and enduring memory trace of attenuated threat in humans.

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Section: Discussionsupporting

confidence: 62%

Rewarded extinction increases amygdalar connectivity and stabilizes long-term memory traces in the vmPFC

Keller

Hennings

Leiker

et al. 2021

Preprint

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show abstract

“…Unexpectedly, the neural activation pattern in the NAc was not significantly impacted by sustained exposure to GC, even if a recent study suggests its causal role in instrumental reward seeking in the CORT model ( Dieterich et al, 2021 ). Similarly, a stronger effect of the GC pharmacological treatment was expected on the VTA neural activation, since its contribution is considered crucial to the modulation of reward-motivated behaviours via associative learning ( Bouarab et al, 2019 ).…”

Section: Discussionmentioning

confidence: 94%

Chronic Distress in Male Mice Impairs Motivation Compromising Both Effort and Reward Processing With Altered Anterior Insular Cortex and Basolateral Amygdala Neural Activation

Cabeza

Ramadan

Cramoisy

et al. 2021

Front. Behav. Neurosci.

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In humans and mammals, effort-based decision-making for monetary or food rewards paradigms contributes to the study of adaptive goal-directed behaviours acquired through reinforcement learning. Chronic distress modelled by repeated exposure to glucocorticoids in rodents induces suboptimal decision-making under uncertainty by impinging on instrumental acquisition and prompting negative valence behaviours. In order to further disentangle the motivational tenets of adaptive decision-making, this study addressed the consequences of enduring distress on relevant effort and reward-processing dimensions. Experimentally, appetitive and consummatory components of motivation were evaluated in adult C57BL/6JRj male mice experiencing chronic distress induced by oral corticosterone (CORT), using multiple complementary discrete behavioural tests. Behavioural data (from novelty suppressed feeding, operant effort-based choice, free feeding, and sucrose preference tasks) collectively show that behavioural initiation, effort allocation, and hedonic appreciation and valuation are altered in mice exposed to several weeks of oral CORT treatment. Additionally, data analysis from FosB immunohistochemical processing of postmortem brain samples highlights CORT-dependent dampening of neural activation in the anterior insular cortex (aIC) and basolateral amygdala (BLA), key telencephalic brain regions involved in appetitive and consummatory motivational processing. Combined, these results suggest that chronic distress-induced irregular aIC and BLA neural activations with reduced effort production and attenuated reward value processing during reinforcement-based instrumental learning could result in maladaptive decision-making under uncertainty. The current study further illustrates how effort and reward processing contribute to adjust the motivational threshold triggering goal-directed behaviours in versatile environments.

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“…Unexpectedly, the neural activation pattern in the NAc was not significantly impacted by sustained exposure to GC, even if a recent study suggests its causal role in instrumental reward-seeking in the CORT model (Dieterich et al, 2021). Similarly, an stronger effect of the GC pharmacological treatment was expected on the VTA neural activation, since its contribution is considered crucial for the modulation of reward motivated behaviours via associative learning (Bouarab et al, 2019).…”

Section: Discussionmentioning

confidence: 92%

Chronic distress in male mice impairs motivation compromising both effort and reward processing with altered anterior insular cortex and basolateral amygdala neural activation

Cabeza

Ramadan

Cramoisy

et al. 2021

Preprint

View full text Add to dashboard Cite

In humans and mammals, effort-based decision-making for monetary or food rewards paradigms contribute to the study of adaptive goal-directed behaviours acquired through reinforcement learning. Chronic distress modelled by repeated exposure to glucocorticoids in rodents induces suboptimal decision-making under uncertainty by impinging on instrumental acquisition and prompting negative valence behaviours. In order to further disentangle the motivational tenets of adaptive decision-making, this study addressed the consequences of enduring distress on relevant effort and reward processing dimensions. Experimentally, appetitive and consummatory components of motivation were evaluated in adult C57BL/6JRj male mice experiencing chronic distress induced by oral corticosterone (CORT), using multiple complementary discrete behavioural tests. Behavioural data (from Novelty Supressed Feeding, operant effort-based choice, Free Feeding and Sucrose Preference tasks) collectively show that behavioural initiation, effort allocation and hedonic appreciation and valuation are altered in mice exposed to several weeks of oral CORT treatment. Additionally, data analysis from FosB immunohistochemical processing of postmortem brain samples highlight a CORT-dependent dampening of neural activation in the anterior insular cortex (aIC) and basolateral amygdala (BLA), key telencephalic brain regions involved in cue appetitive and consummatory motivational processing. Combined, these results suggest that chronic distress-induced irregular aIC and BLA neural activations with reduced effort production and attenuated reward value processing during reinforcement-based instrumental learning could result in maladaptive decision-making under uncertainty. The current study further illustrates how the stoichiometry of effort and reward processing contributes to dynamically adjust the motivational threshold triggering goal-directed behaviours in versatile environments.

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Activation of Basolateral Amygdala to Nucleus Accumbens Projection Neurons Attenuates Chronic Corticosterone-Induced Behavioral Deficits in Male Mice

Cited by 21 publications

References 78 publications

Rewarded extinction increases amygdalar connectivity and stabilizes long-term memory traces in the vmPFC

Rewarded extinction increases amygdalar connectivity and stabilizes long-term memory traces in the vmPFC

Chronic Distress in Male Mice Impairs Motivation Compromising Both Effort and Reward Processing With Altered Anterior Insular Cortex and Basolateral Amygdala Neural Activation

Chronic distress in male mice impairs motivation compromising both effort and reward processing with altered anterior insular cortex and basolateral amygdala neural activation

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