Intra-amygdala anxiogenic drug infusion prior to retrieval biases rats towards the use of habit memory

Elliott, Audrea E.; Packard, Mark G.

doi:10.1016/j.nlm.2008.06.012

Cited by 79 publications

(55 citation statements)

References 58 publications

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“…It appears that participants with higher stressinduced cortisol levels show stronger amygdala activity, especially during the updating of memories, biasing them towards stimulus-response learning. Previous experiments in rodents focused on the effects of a stress-induced shift between memory systems at encoding (Packard and Teather, 1998;Packard and Wingard, 2004;Wingard and Packard, 2008) or retrieval (Elliott and Packard, 2008). Our findings are the first to indicate that also the updating of already encoded (but not yet consolidated) information might be affected by a stress-induced shift in humans.…”

Section: Discussionsupporting

confidence: 49%

“…Whereas earlier studies focused on stress effects on memory quantity, recent studies illustrated that stress also changes memory quality by shifting the balance of systems underlying learning (Hermans et al, 2014;Schwabe and Wolf, 2013b) and retrieval (Elliott and Packard, 2008). Accordingly, memory formation under stress appears to be dominated by inflexible, 'habitual' forms of learning such as stimulusresponse learning based on the striatum.…”

Section: Introductionmentioning

confidence: 99%

“…Under stress, rodents and humans preferentially use simple responses related to salient landmarks that are encoded egocentrically and depend on the striatum (Elliott and Packard, 2008;Kim et al, 2001;Packard and Teather, 1998;Packard and Wingard, 2004;Schwabe et al, 2007;Schwabe et al, 2010;Wingard and Packard, 2008). In contrast, stress impairs more complex, allocentric, spatial representations that are based on the hippocampus (Morris et al, 1982) and allow flexible navigation.…”

Section: Introductionmentioning

confidence: 99%

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Stress Induces a Shift Towards Striatum-Dependent Stimulus-Response Learning via the Mineralocorticoid Receptor

Vogel

Klumpers

Schröder

et al. 2016

Neuropsychopharmacol

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Stress is assumed to cause a shift from flexible 'cognitive' memory to more rigid 'habit' memory. In the spatial memory domain, stress impairs place learning depending on the hippocampus whereas stimulus-response learning based on the striatum appears to be improved. While the neural basis of this shift is still unclear, previous evidence in rodents points towards cortisol interacting with the mineralocorticoid receptor (MR) to affect amygdala functioning. The amygdala is in turn assumed to orchestrate the stress-induced shift in memory processing. However, an integrative study testing these mechanisms in humans is lacking. Therefore, we combined functional neuroimaging of a spatial memory task, stress-induction, and administration of an MR-antagonist in a full-factorial, randomized, placebo-controlled between-subjects design in 101 healthy males. We demonstrate that stress-induced increases in cortisol lead to enhanced stimulusresponse learning, accompanied by increased amygdala activity and connectivity to the striatum. Importantly, this shift was prevented by an acute administration of the MR-antagonist spironolactone. Our findings support a model in which the MR and the amygdala play an important role in the stress-induced shift towards habit memory systems, revealing a fundamental mechanism of adaptively allocating neural resources that may have implications for stress-related mental disorders.

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Section: Discussionsupporting

confidence: 49%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Stress Induces a Shift Towards Striatum-Dependent Stimulus-Response Learning via the Mineralocorticoid Receptor

Vogel

Klumpers

Schröder

et al. 2016

Neuropsychopharmacol

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“…In fact, administration of pretraining stress results in greater use of habit/striatal memory systems compared to spatial/hippocampal memory systems on probe trials in a water maze version of the DST-Maze (Kim et al, 2001). Furthermore, increasing arousal with anxiogenic drugs (e.g., α2 adrenergic receptor antagonists) prior to training or the probe trial on a modification of the water DST-maze leads to a robust use of habit memory systems (Packard and Wingard, 2004, Elliott and Packard, 2008). These observations, coupled with the findings from the present study suggest that other maladaptive behaviors caused by chronic stress may play a role in producing biases towards use of striatal based memory system.…”

Section: Discussionmentioning

confidence: 99%

Chronic stress may facilitate the recruitment of habit- and addiction-related neurocircuitries through neuronal restructuring of the striatum

et al. 2014

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Chronic stress is an established risk factor in the development of addiction. Addiction is characterized by a progressive transition from casual drug use to habitual and compulsive drug use. The ability of chronic stress to facilitate the transition to addiction may be mediated by increased engagement of the neurocircuitries underlying habitual behavior and addiction. In the present study, striatal morphology was evaluated after two weeks of chronic variable stress in male Sprague-Dawley rats. Dendritic complexity of medium spiny neurons was visualized and quantified with Golgi staining in the dorsolateral and dorsomedial striatum, as well as in the nucleus accumbens core and shell. In separate cohorts, the effects of chronic stress on habitual behavior and the acute locomotor response to methamphetamine were also assessed. Chronic stress resulted in increased dendritic complexity in the dorsolateral striatum and nucleus accumbens core, regions implicated in habitual behavior and addiction, while decreased complexity was found in the nucleus accumbens shell, a region critical for the initial rewarding effects of drugs of abuse. Chronic stress did not affect dendritic complexity in the dorsomedial striatum. A parallel shift toward habitual learning strategies following chronic stress was also identified. There was an initial reduction in acute locomotor response to methamphetamine, but no lasting effect as a result of chronic stress exposure. These findings suggest that chronic stress may facilitate the recruitment of habit- and addiction-related neurocircuitries through neuronal restructuring in the striatum.

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“…Consistent with this explanation are recent findings that chronic stress exposure increases habit-based responding, with corresponding atrophy and hypertrophy of goaldirected and habit-based neural circuitry, respectively (DiasFerreira et al 2009). The reliance on habit memory is also increased following anxiogenic drug infusions into the amygdala (Elliott and Packard 2008), which further implicates amygdalar modulatory activity during and after stress exposure in decreasing flexible behavior. If the stress experience did increase perseverative choice behavior, this may partially explain previously observed associations between distress and perseveration in humans (Robinson et al 2006).…”

mentioning

confidence: 87%

Stress impairs optimal behavior in a water foraging choice task in rats

2009

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Stress is a biologically significant social–environmental factor that plays a pervasive role in influencing human and animal behaviors. While stress effects on various types of memory are well characterized, its effects on other cognitive functions are relatively unknown. Here, we investigated the effects of acute, uncontrollable stress on subsequent decision-making performance in rats, using a computer vision-based water foraging choice task. Experiencing stress significantly impaired the animals' ability to progressively bias (but not maintain) their responses toward the larger reward when transitioning from equal to unequal reward quantities. Temporary inactivation of the amygdala during stress, however, blocked impairing effects on decision making.

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Intra-amygdala anxiogenic drug infusion prior to retrieval biases rats towards the use of habit memory

Cited by 79 publications

References 58 publications

Stress Induces a Shift Towards Striatum-Dependent Stimulus-Response Learning via the Mineralocorticoid Receptor

Stress Induces a Shift Towards Striatum-Dependent Stimulus-Response Learning via the Mineralocorticoid Receptor

Chronic stress may facilitate the recruitment of habit- and addiction-related neurocircuitries through neuronal restructuring of the striatum

Stress impairs optimal behavior in a water foraging choice task in rats

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