The adaptive threat bias in anxiety: Amygdala–dorsomedial prefrontal cortex coupling and aversive amplification

Robinson, Oliver J.; Charney, Danielle R.; Overstreet, Cassie; Vytal, Katherine; Grillon, Christian

doi:10.1016/j.neuroimage.2011.11.096

Cited by 186 publications

(263 citation statements)

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“…Analysis of the stimulus onsets in the categorical model (i.e., onset of the face stimuli independent of the parametric modulator) revealed altered activity in regions previously associated with the processing of face stimuli, including the fusiform gyrus and superior temporal sulcus. In the contrast of stress vs. safe, there was significant activity (P whole-brain uncorrected < 0.001) most strongly in the right midoccipital cortex (peak xyz = 46, −64, 28) and the dorsal medial prefrontal cortex (peak xyz = −18, 30, 46), a region we previously implicated in stress responding (11). No regions were more active for safe than stress.…”

Section: Methodsmentioning

confidence: 81%

“…On 25% of trials, this feedback was reversed, leading to either a fear or a happy face PE. Faces were used because they are naturalistic emotional stimuli with privileged aversive and appetitive responses (relative to more secondary, conditioned rewards and punishments, such as money) and because they provide a direct link to our recent work using the same facial stimuli during perception tasks (11,29). [As an aside, we also showed previously that simple "smiley" cartoon happy and sad faces can elicit dissociable striatal PEs (6) that are differentially sensitive to dopamine (30), serotonin (31,32), and major depression (33).…”

Section: Methodsmentioning

confidence: 99%

“…Moreover, the translational model of stress we used is thought to tap into processes contributing to pathological anxiety (11,12). By tying this translational model to computational models of learning, we therefore open the door to uncovering factors involved in the etiology and maintenance of anxiety disorders from a neurocomputational perspective (19).…”

Section: Fig 1 (A)mentioning

confidence: 99%

“…This hypothesis, however, is untested. Therefore, here we used a translational stress induction method in healthy humans (8,(10)(11)(12) to test the hypothesis that stress elevates aversive ventral striatum PE signal.Stress levels were modulated within subjects (n = 24) using a paradigm adapted from rodent studies: threat of foot shock (8,(10)(11)(12). Its impact upon the neural substrates of PE processing was established by recording striatal blood-oxygen-level-dependent (BOLD) signal from individuals completing a simple task designed to elicit matched appetitive (happy face) and aversive (fear face) prediction errors in the absence of behavioral confounds (Fig.…”

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confidence: 99%

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confidence: 99%

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Stress increases aversive prediction error signal in the ventral striatum

Robinson

Overstreet

Charney

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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From job interviews to the heat of battle, it is evident that people think and learn differently when stressed. In fact, learning under stress may have long-term consequences; stress facilitates aversive conditioning and associations learned during extreme stress may result in debilitating emotional responses in posttraumatic stress disorder. The mechanisms underpinning such stress-related associations, however, are unknown. Computational neuroscience has successfully characterized several mechanisms critical for associative learning under normative conditions. One such mechanism, the detection of a mismatch between expected and observed outcomes within the ventral striatum (i.e., "prediction errors"), is thought to be a critical precursor to the formation of new stimulusoutcome associations. An untested possibility, therefore, is that stress may affect learning via modulation of this mechanism. Here we combine a translational model of stress with a cognitive neuroimaging paradigm to demonstrate that stress significantly increases ventral striatum aversive (but not appetitive) prediction error signal. This provides a unique account of the propensity to form threat-related associations under stress with direct implications for our understanding of both normal stress and stress-related disorders.threat of shock | punishment | anxiety | face perception L earning to associate cues with threat is adaptive because it allows future threat to be predicted and avoided (1). However, such associative learning also may lead to haunting and debilitating memories; the smell of stir-fry may evoke painful intrusive memories in Vietnam veterans. How aversive information is integrated to guide adaptive or maladaptive behavior, however, is not well understood. Here, we report that stress increases a key learning mechanism: the neural detection of a mismatch between an expected and observed aversive outcome within the ventral striatum, commonly referred to as the aversive prediction error (PE) signal (1, 2).Neurocomputational and neuroeconomic accounts of cognition posit that stimulus-outcome associations during conditioning are formed via temporal difference learning (1, 3, 4), in which learning depends upon comparing expectation to what is currently happening. New associations, it is argued, are driven by a difference between predicted and actual outcomes (i.e., "prediction errors"), with greater mismatch between expected and actual outcomes evoking greater PE, resulting in greater predictive learning. This mismatch gives rise to phasic dopamine release in the ventral striatum (1, 3-5) for both appetitive and aversive stimuli (1, 2, 6, 7). Little is known, however, about how PE processing might be affected by an organism's emotional state. Stress, for instance, is well known to facilitate aversive conditioning in both humans and animals (8, 9), raising the possibility that aversive PEs also might be increased by stress. This hypothesis, however, is untested. Therefore, here we used a translational stress induction method in healt...

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Section: Methodsmentioning

confidence: 81%

Section: Methodsmentioning

confidence: 99%

Section: Fig 1 (A)mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Stress increases aversive prediction error signal in the ventral striatum

Robinson

Overstreet

Charney

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Oxytocin Differentially Modulates Amygdala Responses during Top‐Down and Bottom‐Up Aversive Anticipation

et al. 2020

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The ability to successfully regulate negative emotions such as fear and anxiety is vital for mental health. Intranasal administration of the neuropeptide oxytocin (OXT) has been shown to reduce amygdala activity but to increase amygdala-prefrontal cortex connectivity during exposure to threatening stimuli suggesting that it may act as an important modulator of emotion regulation. The present randomized, between-subject, placebo-controlled pharmacological study combines the intranasal administration of OXT with functional magnetic resonance imaging (fMRI) during an explicit emotion regulation paradigm in 65 healthy male participants to investigate the modulatory effects of OXT on both bottom-up and top-down emotion regulation. OXT attenuates the activation in the posterior insular cortex and amygdala during anticipation of top-down regulation of predictable threat stimuli in participants with high trait anxiety. In contrast, OXT enhances amygdala activity during the bottom-up anticipation of unpredictable threat stimuli in participants with low trait anxiety. OXT may facilitate top-down goal-directed attention by attenuating amygdala activity in high anxiety individuals, while promoting bottom-up attention/vigilance to unexpected threats by enhancing amygdala activity in low anxiety individuals. OXT may thus have the potential to promote an adaptive balance between bottom-up and top-down attention systems depending on an individual's trait anxiety level.

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The benefits of bivalve reef restoration: A global synthesis of underrepresented species

Ermgassen

Thurstan

Corrales

et al. 2020

Aquatic Conservation

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Bivalve habitat restoration is growing in geographic extent and scale globally. While addressing the wide‐scale loss of these biogenic habitats is still a key motivation behind restoration efforts, stakeholders and funders are increasingly drawn to shellfish restoration for the many ecosystem services these habitats provide. There is clear evidence for the provision of ecosystem services from species targeted for restoration in the USA, in particular Crassostrea virginica. Ecosystem services, however, remain largely unquantified or even undescribed for the majority of other species targeted for restoration. A structured review of the literature was undertaken and supplemented by expert knowledge to identify which ecosystem services are documented in the following other bivalve species targeted for restoration: Ostrea edulis, Ostrea angasi, Crassostrea rhizophorae, Perna canaliculus, Modiolus modiolus, Mytilus edulis, Mytilus platensis, Crassostrea gigas, Ostrea denselamellosa, Crassostrea ariakensis, and Crassostrea sikamea. Key knowledge gaps in quantifying ecosystem services and the ecosystem engineering properties of habitat‐building bivalves contributing to the provision of ecosystem services were identified. Ecosystem services with the potential to be widely applicable across bivalve habitat‐building species were identified. Though there is evidence that many of the ecosystem engineering properties that underpin the provision of ecosystem services are universal, the degree to which services are provided will vary between locations and species. Species‐specific, in situ, studies are needed in order to avoid the inappropriate transfer of the ecosystem service delivery between locations, and to further build support and understanding for these emerging targets of restoration.

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The adaptive threat bias in anxiety: Amygdala–dorsomedial prefrontal cortex coupling and aversive amplification

Cited by 186 publications

References 36 publications

Stress increases aversive prediction error signal in the ventral striatum

Stress increases aversive prediction error signal in the ventral striatum

Oxytocin Differentially Modulates Amygdala Responses during Top‐Down and Bottom‐Up Aversive Anticipation

The benefits of bivalve reef restoration: A global synthesis of underrepresented species

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