Neural traces of stress: cortisol related sustained enhancement of amygdala-hippocampal functional connectivity (original) (raw)
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NeuroImage, 2010
Recent neuroimaging studies investigating responses to stressful stimuli may importantly further our understanding of psychological trauma etiology. However, theory posits that sustained activation of these stress circuits after the stressful event may play an equally important role in the development of stressrelated psychopathology. Importantly, such post-stress network changes remain poorly characterized. The amygdala with its connections is crucially positioned in the central stress circuitry that mediates the initial stress response. Hence, we investigated post-stress amygdala-centered connectivity patterns in order to characterize the aftermath of acute, experimentally-induced stress in healthy humans. We recorded restingstate functional MRI in 26 female participants following a period of moderate psychological stress induced by means of aversive (vs. emotionally neutral) movie watching with a self-referencing instruction. Next, we implemented a seedregion analysis calculating the voxel-wise correlation with the anatomically extracted time-series of the amygdala. Various stress measures confirmed successful stress induction. Moreover, we demonstrated enhanced functional coupling of the amygdala with dorsal anterior cingulate cortex, anterior insula, and a dorso-rostral pontine region, which appears to overlap with the anatomical location of the locus coeruleus (LC), when contrasting the stress with the control group. Thus, we show that the aftermath of acute stress is qualified by prolonged activation in an amygdala-connectivity network. This pattern of coactivation may indicate an extended state of hypervigilance that promotes sustained salience and mnemonic processing after stress. Characterization of the post-stress brain state may provide initial insight into the early phases of psychological trauma formation.
European Journal of Neuroscience, 2021
Abundant evidence shows that early-life stress (ELS) predisposes for the development of stress-related psychopathology when exposed to stressors later in life, but the underlying mechanisms remain unclear. To study predisposing effects of mild ELS on stress sensitivity, we examined in a healthy human population the impact of a history of ELS on acute stress-related changes in corticolimbic circuits involved in emotional processing (i.e., amygdala, hippocampus and ventromedial prefrontal cortex [vmPFC]). Healthy young male participants (n = 120) underwent resting-state functional magnetic resonance imaging (fMRI) in two separate sessions (stress induction vs. control). The Childhood Trauma Questionnaire (CTQ) was administered to index selfreported ELS, and stress induction was verified using salivary cortisol, blood pressure, heart rate and subjective affect. Our findings show that self-reported ELS was negatively associated with baseline cortisol, but not with the acute stress-induced cortisol response. Critically, individuals with more self-reported ELS exhibited an exaggerated reduction of functional connectivity in corticolimbic circuits under acute stress. A mediation analysis showed that the association between ELS and stress-induced changes in amygdalahippocampal connectivity became stronger when controlling for basal cortisol. Our findings show, in a healthy sample, that the effects of mild ELS on functioning of corticolimbic circuits only become apparent when exposed to an acute stressor and may be buffered by adaptations in hypothalamic-pituitaryadrenal axis function. Overall, our findings might reveal a potential
NeuroImage, 2011
Whereas we know a fair amount on the role of the amygdala in the acute stress response, virtually nothing is known about its role during the recovery period after the stress has waned. Functional connectivity analysis of the amygdala during this period might be useful in revealing brain circuits promoting adaptive recovery from a stressful event, as well as consolidation of emotionally relevant information in preparing for future challenges. Healthy participants were randomly assigned to either a psychosocial stress task (n = 18; stress group) or a comparable non-stressful control procedure (n = 20; controls). To study the prolonged effects of stress on amygdala functional connectivity, resting-state fMRI scans were acquired an hour after the stress task. Amygdala functional connectivity with other brain regions was assessed using seed-based correlations. The stress group exhibited a strong physiological and behavioral reaction to psychosocial stress exposure. Compared with controls the stress group showed increased amygdala functional connectivity with three cortical midline structures: the posterior cingulate cortex and precuneus (p b .05, corrected), and the medial prefrontal cortex (p b .05, small volume corrected). An hour after psychosocial stress, changes in amygdala functional connectivity were detected with cortical midline structures involved in the processing and regulation of emotions, as well as autobiographical memory. It is hypothesized that these effects could relate to top-down control of the amygdala and consolidation of self-relevant information after a stressful event. These results on functional connectivity in the recovery phase after stress might provide an important new vantage point in studying both sensitivity and resilience to stress.
Acute stress alters the ‘default’ brain processing
NeuroImage, 2019
Active adaptation to acute stress is essential for coping with daily life challenges. The stress hormone cortisol, as well as large scale reallocations of brain resources have been implicated in this adaptation. Stress-induced shifts between large-scale brain networks, including salience (SN), central executive (CEN) and default mode networks (DMN), have however been demonstrated mainly under task-conditions. It remains unclear whether such network shifts also occur in the absence of ongoing task-demands, and most critically, whether these network shifts are predictive of individual variation in the magnitude of cortisol stress-responses. In a sample of 335 healthy participants, we investigated stress-induced functional connectivity changes (delta-FC) of the SN, CEN and DMN, using resting-state fMRI data acquired before and after a socially evaluated coldpressor test and a mental arithmetic task. To investigate which network changes are associated with acute stress, we evaluated the association between cortisol increase and delta-FC of each network. Stress-induced cortisol increase was associated with increased connectivity within the SN, but with decreased coupling of DMN at both local (within network) and global (synchronization with brain regions also outside the network) levels. These findings indicate that acute stress prompts immediate connectivity changes in large-scale resting-state networks, including the SN and DMN in the absence of explicit ongoing task-demands. Most interestingly, this brain reorganization is coupled with individuals' cortisol stress-responsiveness. These results suggest that the observed stress-induced network reorganization might function as a neural mechanism determining individual stress reactivity and, therefore, it could serve as a promising marker for future studies on stress resilience and vulnerability.
2021
Acute stress in a long period of time could drastically influence one's behavioral and cognitive performances. Therefore, it is important to control the stressful situation and release it after a stressful event. In this regard, understanding of brain mechanism of the stress release will help to introduce new practical approaches. In this study, we hypothesized that induction and release of stress will change the brain functional connectivity pattern. Therefore, by recruiting 20 healthy-subjects and exposing them to stressful events using the trier social stress paradigm, we aimed to investigate patterns of these changes. In a session consist of 23 minutes of psychological stress induction and 20 minutes of recovery, subjects' stress was scored by visual analogue scale (VAS). In addition, salivary cortisol level and EEG data of the subjects were also recorded. Subsequently, brain functional connectivity (FC) maps were calculated in a frequency-specific manner. Then, the effe...
A large-scale perspective on stress-induced alterations in resting-state networks
Scientific Reports, 2016
Stress is known to induce large-scale neural modulations. However, its neural effect once the stressor is removed and how it relates to subjective experience are not fully understood. Here we used a statistically sound data-driven approach to investigate alterations in large-scale resting-state functional connectivity (rsFC) induced by acute social stress. We compared rsfMRI profiles of 57 healthy male subjects before and after stress induction. Using a parcellation-based univariate statistical analysis, we identified a large-scale rsFC change, involving 490 parcel-pairs. Aiming to characterize this change, we employed statistical enrichment analysis, identifying anatomic structures that were significantly interconnected by these pairs. This analysis revealed strengthening of thalamo-cortical connectivity and weakening of cross-hemispheral parieto-temporal connectivity. These alterations were further found to be associated with change in subjective stress reports. Integrating report-based information on stress sustainment 20 minutes post induction, revealed a single significant rsFC change between the right amygdala and the precuneus, which inversely correlated with the level of subjective recovery. Our study demonstrates the value of enrichment analysis for exploring large-scale network reorganization patterns, and provides new insight on stress-induced neural modulations and their relation to subjective experience. Acute stress has been shown to have dramatic effects on the way our brain functions, which can be viewed as a strategic resource reallocation to functions that are required when facing a threat such as promoting arousal 1,2 and memory encoding of stressful experiences 3-5 , at the cost of higher cognitive functions 6-8. However, while the neural basis of the stress response at the time of induction has been widely investigated, less is known about the neural processes that underlie successive recovery in humans. Characterizing individual variability in recovery from stress is of a particular interest since it has been associated with several stress-related psychopathologies, including Post Traumatic Stress Disorder (PTSD) and depression 9,10. One approach to study post-processing of prior events, such as stress, is by inspecting the spontaneous neural activity that takes place during rest after the event occurred. It has been suggested that this post-processing supports prior experience consolidation 11-13 , and thus, may play a central role in regaining mental and physiological homeostasis, and is expected to involve large scale brain network reorganization 14-16. Accordingly, using post-stress resting-state functional magnetic resonance imaging (rsfMRI) to investigate network reorganization following stress may provide a vital insight into the large-scale neural mechanism that underlies affective recovery from acute stress. Few previous fMRI studies investigated changes in resting-state functional connectivity (rsFC) following acute stress 17-19. For example, van Marle et al. reported increased amygdala rsFC immediately following acute stress with anterior cingulate cortex, anterior insula, and a dorso-rostral pontine region 18. In another study Veer et al. reported increased amygdala rsFC with the posterior cingulate cortex (PCC), precuneus and medial prefrontal cortex an hour following stress, suggesting that these effects could be related to top-down control of the amygdala and consolidation of self-relevant information following a stressful event 19. Lastly, Vaisvaser et al. 17 examined changes in rsFC patterns seeded at the PCC and hippocampus. Unlike the two aforementioned studies, here rsFC
Stress Impact on Resting State Brain Networks
PLoS ONE, 2013
Resting state brain networks (RSNs) are spatially distributed large-scale networks, evidenced by resting state functional magnetic resonance imaging (fMRI) studies. Importantly, RSNs are implicated in several relevant brain functions and present abnormal functional patterns in many neuropsychiatric disorders, for which stress exposure is an established risk factor. Yet, so far, little is known about the effect of stress in the architecture of RSNs, both in resting state conditions or during shift to task performance. Herein we assessed the architecture of the RSNs using functional magnetic resonance imaging (fMRI) in a cohort of participants exposed to prolonged stress (participants that had just finished their long period of preparation for the medical residence selection exam), and respective gender-and age-matched controls (medical students under normal academic activities). Analysis focused on the pattern of activity in resting state conditions and after deactivation. A volumetric estimation of the RSNs was also performed. Data shows that stressed participants displayed greater activation of the default mode (DMN), dorsal attention (DAN), ventral attention (VAN), sensorimotor (SMN), and primary visual (VN) networks than controls. Importantly, stressed participants also evidenced impairments in the deactivation of resting statenetworks when compared to controls. These functional changes are paralleled by a constriction of the DMN that is in line with the pattern of brain atrophy observed after stress exposure. These results reveal that stress impacts on activationdeactivation pattern of RSNs, a finding that may underlie stress-induced changes in several dimensions of brain activity.
Chronic social stress: effects on limbic brain structures
Physiology & Behavior, 2003
Different types of stressors are known to activate distinct neuronal circuits in the brain. Acute physiological stimuli that are life threatening and require immediate reactions lead to a rapid stimulation of brainstem and hypothalamus to activate efferent visceral pathways. In contrast, psychological stressors activate higher-order brain structures for further interpretations of the perceived endangerment. Common to the later multimodal stressors is that they need cortical processing and, depending on previous experience or ongoing activation, the information is assembled within limbic circuits connecting, e.g., the hippocampus, amygdala and prefrontal cortex to induce neuroendocrine and behavioral responses. In view of the fact that stressful life events often contribute to the etiology of psychopathologies such as depressive episodes, several animal models have been developed to study central nervous mechanisms that are induced by stress. The present review summarizes observations made in the tree shrew chronic psychosocial stress paradigm with particular focus on neurotransmitter systems and structural changes in limbic brain regions. D
The brain and the stress axis: The neural correlates of cortisol regulation in response to stress
Neuroimage, 2009
The hypothalamic-pituitary-adrenal (HPA) axis is the major endocrine stress axis of the human organism. Cortisol, the final hormone of this axis, affects metabolic, cardiovascular and central nervous systems both acutely and chronically. Recent advances in neuroimaging techniques have led to the investigation of regulatory networks and mechanisms of cortisol regulation in the central nervous system in human populations. In the following review, results from human and animal studies are being presented that investigate the specific role of hippocampus (HC), amygdala (AG), prefrontal cortex (PFC), and brainstem nuclei in cortisol regulation in response to stress. In general, the types of stressors need to be distinguished when discussing the contributions of these structures in regulating the HPA axis. We propose a basic framework on how these structures communicate as a network to regulate cortisol secretion in response to psychological stress. Furthermore, we review critical studies that have substantially contributed to the literature. Possible future research avenues in the field of neuroimaging of cortisol regulation are discussed. In combination with investigations on genetic and environmental factors that influence the development of the HPA axis, this emerging new research will eventually allow the formulation of a more comprehensive framework of functional neuroanatomy of cortisol regulation.