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A dual-pathway architecture enables chronic stress to promote habit formation.

ABSTRACT: Chronic stress can change how we learn and, thus, how we make decisions by promoting the formation of inflexible, potentially maladaptive, habits. Here we investigated the neuronal circuit mechanisms that enable this. Using a multifaceted approach in male and female mice, we reveal a dual pathway, amygdala-striatal, neuronal circuit architecture by which a recent history of chronic stress shapes learning to disrupt flexible goal-directed behavior in favor of inflexible habits. Chronic stress inhibits activity of basolateral amygdala projections to the dorsomedial striatum to impede the action-outcome learning that supports flexible, goal-directed decisions. Stress also increases activity in direct central amygdala projections to the dorsomedial striatum to promote the formation of rigid, inflexible habits. Thus, stress exerts opposing effects on two amygdala-striatal pathways to promote premature habit formation. These data provide neuronal circuit insights into how chronic stress shapes learning and decision making, and help understand how stress can lead to the disrupted decision making and pathological habits that characterize substance use disorders and other psychiatric conditions.

SUBMITTER: Giovanniello JR

PROVIDER: S-EPMC10592885 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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A dual-pathway architecture enables chronic stress to disrupt agency and promote habit formation.

Giovanniello Jacqueline R JR Paredes Natalie N Wiener Anna A Ramírez-Armenta Kathia K Oragwam Chukwuebuka C Uwadia Hanniel O HO Yu Abigail L AL Lim Kayla K Pimenta Jenna S JS Vilchez Gabriela E GE Nnamdi Gift G Wang Alicia A Sehgal Megha M Reis Fernando McV FM Sias Ana C AC Silva Alcino J AJ Adhikari Avishek A Malvaez Melissa M Wassum Kate M KM

bioRxiv : the preprint server for biology 20240924

Chronic stress can change how we learn and, thus, how we make decisions. Here we investigated the neuronal circuit mechanisms that enable this. Using a multifaceted systems neuroscience approach in male and female mice, we reveal a dual pathway, amygdala-striatal neuronal circuit architecture by which a recent history of chronic stress disrupts the action-outcome learning underlying adaptive agency and promotes the formation of inflexible habits. We found that the basolateral amygdala projection ...[more]

PMID: 37873076

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Project description:Simple Summary Horse training exposes horses to many difficult learning challenges, including tasks that run counter to their natural behaviour and research from neuroscience can be used to understand how horses respond to these learning challenges. Horses can also quickly develop habits, however if the habit is undesirable, the horse may be subjected to retraining where it must learn to suppress the unwanted behaviour and learn a new response. This is called cognitive flexibility and is underpinned by complex neural processes and can be impaired by exposure to repeated or chronic stress. We trained horses to acquire habit-like responses in one of two industry-style aversive instrumental learning scenarios (moving away from the stimulus-instinctual-IS or moving towards the stimulus-non-instinctual-NIS) and evaluated the effect of repeated stress exposures on their cognitive flexibility in a reversal task. We measured heart rate, salivary cortisol and serum brain derived neurotrophic factor to infer possible neural correlates of the learning outcomes. Horses trained in the NIS task took longer to learn task than the horses trained in the IS task, however they were quicker to learn the IS task during the reversal. There was no significant effect of the stress exposures on cognitive flexibility, however the stress did make horses more sensitive to the aversive training stimuli. These results provide guidance for trainers to adapt their practices when training tasks that are difficult for horses to learn and during retraining. In particular, even when horses have been trained to approach aversive stimuli they can quickly learn to avoid them. This has implications for retraining unwanted responses during aversive situations such as trailer loading. Abstract Horse training exposes horses to an array of cognitive and ethological challenges. Horses are routinely required to perform behaviours that are not aligned to aspects of their ethology, which may delay learning. While horses readily form habits during training, not all of these responses are considered desirable, resulting in the horse being subject to retraining. This is a form of cognitive flexibility and is critical to the extinction of habits and the learning of new responses. It is underpinned by complex neural processes which can be impaired by chronic or repeated stress. Domestic horses may be repeatedly exposed to multiples stressors. The potential contribution of stress impairments of cognitive flexibility to apparent training failures is not well understood, however research from neuroscience can be used to understand horses’ responses to training. We trained horses to acquire habit-like responses in one of two industry-style aversive instrumental learning scenarios (moving away from the stimulus-instinctual or moving towards the stimulus-non-instinctual) and evaluated the effect of repeated stress exposures on their cognitive flexibility in a reversal task. We measured heart rate as a proxy for noradrenaline release, salivary cortisol and serum Brain Derived Neurotrophic Factor (BDNF) to infer possible neural correlates of the learning outcomes. The instinctual task which aligned with innate equine escape responses to aversive stimuli was acquired significantly faster than the non-instinctual task during both learning phases, however contrary to expectations, the repeated stress exposure did not impair the reversal learning. We report a preliminary finding that serum BDNF and salivary cortisol concentrations in horses are positively correlated. The ethological salience of training tasks and cognitive flexibility learning can significantly affect learning in horses and trainers should adapt their practices where such tasks challenge innate equine behaviour.

Project description:BackgroundInterventions aimed at promoting physical activity (PA) behavior through habit formation pathways are gaining popularity, as they differ from conventional interventions that rely on intention pathways. Past research has established a positive correlation between PA habits and behavior. However, the efficacy of current interventions designed to form PA habits and improve PA automaticity is not yet fully ascertained. Additionally, the intervention components that significantly impact the effectiveness of these interventions are yet to be determined.MethodsThis systematic review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. We conducted a search of three databases (PubMed, Embase, and Cochrane Library) from January 2000 to December 2022, with a focus on interventions for developing PA habits. Two independent authors conducted paper selection, quality assessment, data extraction, and coding of behavior change techniques (BCTs). The effect size of interventions was calculated using standardized mean difference. Subgroup analyses were carried out based on follow-up duration, delivery method, sample characteristics, and theory. Furthermore, we employed meta-regression to investigate the association between BCTs and PA habits.ResultsTen eligible studies with relatively high quality were included in the final data set. Characteristics of studies varied in intervention sample and delivery way. The habit formation interventions significantly increased PA habit (SMD = 0.31, 95% CI 0.14-0.48, P < .001) compared to the control groups. Subgroup analysis demonstrated that the duration of follow-up ≤ 12 weeks have a higher effect size on PA habit than the duration > 12 weeks. Meta-regression revealed that problem solving has a significant positive association with effectiveness improvement (β = 0.36, 95% CI 0.17-0.55), while social reward is linked with a reduction in effectiveness (β = -0.40, 95% CI -0.74-0.06).ConclusionsOur findings reveal that habit formation interventions are effective in fostering PA habit. Future studies could leverage the insights form this study to optimize the intervention design and achieve better effectiveness.

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A dual-pathway architecture enables chronic stress to promote habit formation.

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A dual-pathway architecture enables chronic stress to disrupt agency and promote habit formation.

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