Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress

Marle, Hein J. F. van; Hermans, Erno J.; Qin, Shaozheng; Fernández, Guillén

doi:10.1016/j.neuroimage.2010.05.070

Cited by 224 publications

(196 citation statements)

References 53 publications

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“…This might suggest that the stress-induced enhancement of amygdala activity might take about twenty minutes to arise which would be in line with in-vitro findings of enhanced amygdala excitability after corticosterone applications of 20 min (Karst et al, 2010) and a delayed rise of brain corticosterone levels after stress (Qian et al, 2011). Furthermore, the stress-induced increase in amygdala activity and connectivity may be transient as amygdala activity was found to be reduced one hour after hydrocortisone administration (Henckens et al, 2010) and no connectivity increase with the striatum could be detected one hour after stress onset (van Marle et al, 2010) or hydrocortisone administration (Henckens et al, 2012). These results highlight the striking time-dependency of stress effects on neural activity and memory (Henckens et al, 2010;Joëls et al, 2011;van Ast et al, 2013).…”

Section: Discussionsupporting

confidence: 70%

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: 70%

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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“…All participants were right-handed men between 21 and 37 years old. The mean age of the partici pants was 27.3 (SD 4.5) years in the PTSD group and 26.6 (SD 3.3) years in the control group (t 26 …”

Section: Resultsmentioning

confidence: 99%

“…19 The amygdala and insula are structurally interconnected, 23 and early PET studies reported increased insula activity in response to trauma script-driven imagery in individuals with PTSD, 24 though in some studies no more than in combat-exposed controls. 25 Recent fMRI studies have reported greater insula activation in anticipation of negative images 19 and negative emotional faces 18 in individuals with PTSD as well as enhanced coupling between the insula and amygdala during negative emotion induction in healthy volunteers 26 and during symptom provocation in recently traumatized individuals. 16 Etkin and Wager's meta-analysis 10 also suggests coactivation of the right amygdala and insula across studies, and collectively these studies offer evidence of strong anatomic and functional links between the amygdala and insula during emotion processing.…”

Section: Introductionmentioning

confidence: 99%

Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder

Sripada

King

Garfinkel

et al. 2012

jpn

311

289

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IntroductionPosttraumatic stress disorder (PTSD) is a debilitating psychiatric disorder characterized by symptoms of re-experiencing, hyperarousal, emotional numbing and avoidance; 1 however, exact brain mechanisms involved in the generation of PTSD symptoms or in PTSD pathophysiology have yet to be elucidated. Converging neuroimaging research points to a potentially critical role for disrupted emotion neurocircuitry in individuals with PTSD, and whereas many studies have delineated patterns of activations during face viewing or symptom provocation (for a review, see Shin and Liberzon 2 ), relatively few have examined patterns of connectivity in the brains of patients with PTSD at rest, a potentially powerful method for illuminating brain network structure. 3,4 Most PTSD neuroimaging studies to date have described abnormalities in emotion-generation regions, such as the amygdala or insula, and emotion-regulation regions, including the anterior cingulate cortex (ACC) and medial prefrontal cortex (mPFC). This is consistent with the known role of the amygdala as a key region in threat detection, 5 fear conditioning 6 and emotional salience, 7 and of the mPFC as a modulatory region interconnected with limbic structures 8 and involved in emotion regulation.9 Taken together, functional magnetic resonance imaging (fMRI) studies of individuals with PTSD suggest patterns of hyperactivation of the amygdala and insula to emotion-related stimuli and corresponding hypoactivation of ventromedial prefrontal and rostral anterior cingulate cortices.2 This pattern of amygdala hyperactivity and mPFC hypoactivity was recently confirmed by a meta-analysis of 15 PTSD neuroimaging studies 10 and is generally understood to reflect a lack of regulatory control over emotion in individuals with PTSD.Studies of functional connectivity, however, can provide additional and potentially more direct information about regu latory relationships between the mPFC and amygdala. The amygdala has tight structural connections and reciprocal feedback loops with the mPFC and orbitofrontal cortex 11 as well as with the dorsolateral PFC 12 and ACC. 13 As amygdala Background: Converging neuroimaging research suggests altered emotion neurocircuitry in individuals with posttraumatic stress disorder (PTSD). Emotion activation studies in these individuals have shown hyperactivation in emotion-related regions, including the amygdala and insula, and hypoactivation in emotion-regulation regions, including the medial prefrontal cortex (mPFC) and anterior cingulate cortex (ACC). However, few studies have examined patterns of connectivity at rest in individuals with PTSD, a potentially powerful method for illuminating brain network structure. Methods: Using the amygdala as a seed region, we measured resting-state brain connectivity using 3 T functional magnetic resonance imaging in returning male veterans with PTSD and combat controls without PTSD. Results: Fifteen veterans with PTSD and 14 combat controls enrolled in our study. Compared with controls, veterans with ...

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“…This observation is reflected by coactivation of the dACC and the anterior insular cortex that form a salience network (57). Functional connectivity studies demonstrate a prolonged enhanced functional coupling in the resting state between amygdala, dACC, anterior insula, and the sympathetic locus coeruleus after psychological stress, resulting in an extended state of hypervigilance that promotes sustained salience and mnemonic processing (87). Thus, the efficient encoding of aversive emotional memories can lead to the formation of a strong, aversive memory trace (88).…”

Section: Phantom Percepts and Memorymentioning

confidence: 99%

Phantom percepts: Tinnitus and pain as persisting aversive memory networks

Ridder¹,

Elgoyhen

Romo

et al. 2011

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

524

456

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Phantom perception refers to the conscious awareness of a percept in the absence of an external stimulus. On the basis of basic neuroscience on perception and clinical research in phantom pain and phantom sound, we propose a working model for their origin. Sensory deafferentation results in high-frequency, gamma band, synchronized neuronal activity in the sensory cortex. This activity becomes a conscious percept only if it is connected to larger coactivated "(self-)awareness" and "salience" brain networks. Through the involvement of learning mechanisms, the phantom percept becomes associated to distress, which in turn is reflected by a simultaneously coactivated nonspecific distress network consisting of the anterior cingulate cortex, anterior insula, and amygdala. Memory mechanisms play a role in the persistence of the awareness of the phantom percept, as well as in the reinforcement of the associated distress. Thus, different dynamic overlapping brain networks should be considered as targets for the treatment of this disorder.A fundamental concept in psychology and philosophy of the mind is the notion of perception: The act of interpreting and organizing a sensory stimulus to produce a meaningful experience of the world and of oneself. A stimulus produces an effect on the different sensory receptors, inducing sensation. Further processing of this sensory stimulation generates an internal representation of the outer and inner world called a percept. Since the first days of psychology, two challenging questions have existed: How is sensory information encoded and, in particular, how is this represented information transformed into the individual awareness of a conscious percept (1)? Our understanding of sensory encoding, perception, and consciousness is challenged with a further degree of complexity in the case of phantom perception, the conscious awareness of a percept in the absence of an external stimulus. Deciphering the underlying neural correlates of phantom perception is a scientific endeavor that will aid in understanding the active processes of selecting, organizing, and interpreting information, which ultimately lead to the formation of a conscious percept within the brain.Although some cases of phantom percepts have been described for the visual, olfactory, and gustatory systems, the vast majority of sensory phantoms are those present in the somatosensory (phantom limb perception/phantom limb pain and neuropathic pain) (2) and auditory (tinnitus) (3) modalities. Upfront we are challenged with the following questions: In the absence of an external sensory stimulus, where and how in the brain is the conscious percept generated? In addition, are the neural substrates underlying the generation of a conscious phantom percept similar for the auditory and somatosensory modalities? If so, can we advance in our understanding and treatment of tinnitus on the basis of what is known for phantom limb and phantom pain perception and vice versa? Here, we address these questions and propose a working model of how pha...

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Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress

Cited by 224 publications

References 53 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

Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder

Phantom percepts: Tinnitus and pain as persisting aversive memory networks

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