How the brain connects in response to acute stress: A review at the human brain systems level

Oort, Jasper van; Tendolkar, Indira; Hermans, Erno J.; Mulders, Peter; Beckmann, Christian F.; Schene, Aart H.; Fernández, Guillén; Eijndhoven, Philip van

doi:10.1016/j.neubiorev.2017.10.015

Cited by 190 publications

(177 citation statements)

References 83 publications

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“…It indicated that patients with pED had different CEN-DMN connectivity models from healthy subjects. Similarly, the weak CEN-DMN connectivity was also detected at many other psychosocial disorders, such as major depression (93), PTSD (94), and acute stress (95). Therefore, based on the previous findings and our current results, we put forward the deduction that patients with pED had decreased synchronous activity between the CEN and the DMN.…”

Section: Discussionsupporting

confidence: 67%

Associations Between Altered Cerebral Activity Patterns and Psychosocial Disorders in Patients With Psychogenic Erectile Dysfunction: A Mediation Analysis of fMRI

Yin

Liu

et al. 2020

Front. Psychiatry

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Previous studies had illustrated the significant neural pathological changes in patients with psychogenic erectile dysfunction (pED), while few works focused on the neural underpinning of the psychosocial status in patients with pED. This study aimed to investigate the associations among the altered cerebral activity patterns, impaired erectile function, and the disrupted psychosocial status in patients with pED. Thirty-two patients with pED and 28 healthy controls (HCs) were included. The amplitude of low-frequency fluctuations (ALFF), region-of-interest-based functional connectivity (FC), as well as Pearson correlation analyses and mediation analyses between neuroimaging outcomes and clinical outcomes were performed. Compared to HCs, patients with pED manifested lower erectile function, disrupted psychosocial status, as well as decreased ALFF in the left dorsolateral prefrontal cortex (dlPFC) and reduced FC between the left dlPFC and left angular gyrus, and left posterior cingulate cortex (PCC) and precuneus, which belonged to the default mode network (DMN). Moreover, both the ALFF of the left dlPFC and FC between the left dlPFC and left PCC and precuneus were significantly correlated with the sexual function and psychosocial status in patients with pED. The disrupted psychosocial status mediated the influence of atypical FC between dlPFC and DMN on decreased erectile function. This study widened our understanding of the important role of psychosocial disorders in pathological neural changes in patients with pED.

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Section: Discussionsupporting

confidence: 67%

Associations Between Altered Cerebral Activity Patterns and Psychosocial Disorders in Patients With Psychogenic Erectile Dysfunction: A Mediation Analysis of fMRI

Yin

Liu

et al. 2020

Front. Psychiatry

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“…Our data are well in line with findings in humans where acute stress exposures (induced by aversive movies or social stressors) were followed by a significant increase of FC in the Salience Network 30 and Default Mode Network 79 . Similarly, task-based fMRI reveals that acute stress leads to increased interconnectivity and positive BOLD responses within several cortical regions related to salience processing (frontoinsular, anterior cingulate, inferotemporal, and temporoparietal) and subcortical regions (amygdala, striatum, thalamus, hypothalamus, hippocampus and midbrain) as a function of stress response magnitude 31,[80][81][82] . Notably, increased connectivity in the Salience Network was blocked by systemic administration of a beta-adrenergic receptor antagonist (propranolol) 31 .…”

Section: Lc Activation Recapitulates Many Of the Complex Effects Trigmentioning

confidence: 99%

Rapid Reconfiguration of the Functional Connectome after Chemogenetic Locus Coeruleus Activation

Zerbi

Floriou-Servou

Markicevic

et al. 2019

Preprint

107

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The locus coeruleus (LC) supplies norepinephrine (NE) to the entire forebrain, regulates many fundamental brain functions, and is implicated in several neuropsychiatric diseases. Although selective manipulation of the LC is not possible in humans, studies have suggested that strong LC activation might shift network connectivity to favor salience processing. To test this hypothesis, we use a mouse model to study the impact of LC stimulation on large-scale functional connectivity by combining chemogenetic activation of the LC with resting-state fMRI, an approach we term "chemo-connectomics". LC activation rapidly interrupts ongoing behavior and strongly increases brain-wide connectivity, with the most profound effects in the salience and amygdala networks. We reveal a direct correlation between functional connectivity changes and transcript levels of alpha-1, alpha-2, and beta-1 adrenoceptors across the brain, and a positive correlation between NE turnover and functional connectivity within select brain regions. These results represent the first brain-wide functional connectivity mapping in response to LC activation, and demonstrate a causal link between receptor expression, brain states and functionally connected large-scale networks at rest. We propose that these changes in large-scale network connectivity are critical for optimizing neural processing in the context of increased vigilance and threat detection. RESULTSTo selectively target the LC, we used transgenic mice that express codon-improved Crerecombinase (iCre) under the dopamine-beta-hydroxylase (DBH) promoter (DBH-iCre mice, Figure 1A) 33 . We stereotactically delivered floxed excitatory DREADDs 34 (AAV5-hSyn-DIO-hM3Dq-mCherry; hM3Dq-mCh) or a control virus (AAV5-hSyn-DIO-mCherry; mCh) to the LC, thus restricting virus expression to DBH-positive noradrenergic neurons of the LC (Figure 1B). We assessed successful LC activation using pupillometry, a highly sensitive and clinically relevant readout of LC activation [35][36][37] . After two minutes of baseline recording under light isoflurane anesthesia, we activated LC neurons by administering the potent DREADD activator clozapine at an ultra-low dose (0.03 mg/kg, i.p., Figure 1C) 38 . Within a minute of clozapine injection, we observed a strong increase in pupil diameter in the hM3Dq-mCh group, while pupil diameter of mCh mice did not change in response to clozapine injection and remained stable throughout the 10-minute recording session (Figure 1D-F). To show that our LC activation protocol is behaviorally relevant, we subjected mice to an open field test (OFT) immediately after clozapine injection and recorded their behavior for 30 minutes. In comparison to mCh mice, clozapine injection had profound effects on the behavior of hM3Dq-mCh mice. Several minutes after clozapine administration, hM3Dq-mCh mice showed strongly suppressed locomotor activity ( Figure 1G, H), spent less time in the (more aversive) center of the open field (Figure 1I, J), performed less activity-related supported rears (Figure 1...

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“…HRV as measured by the root mean square of successive differences between normal heartbeats (RMSSD) or high frequency (HF) power are suppressed as a reaction to acute stress induction (Kim et al, 2018;Castaldo et al, 2019). Three dominant brain networks, namely DMN, CEN, and SN, are known to be modulated by acute stress (Hermans et al, 2011;Vaisvaser et al, 2013;Maron-Katz et al, 2016;van Oort et al, 2017). For example, during acute stress induction by affective stimuli, the activation and functional connectivity of SN as well as the activation in DMN regions increase, while the activation in CEN remains unchanged (van Oort et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Heart Rate Variability as an Index of Differential Brain Dynamics at Rest and After Acute Stress Induction

Chand

Jamalabadi

et al. 2020

Front. Neurosci.

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The brain continuously receives input from the internal and external environment. Using this information, the brain exerts its influence on both itself and the body to facilitate an appropriate response. The dynamic interplay between the brain and the heart and how external conditions modulate this relationship deserves attention. In high-stress situations, synchrony between various brain regions such as the prefrontal cortex and the heart may alter. This flexibility is believed to facilitate transitions between functional states related to cognitive, emotional, and especially autonomic activity. This study examined the dynamic temporal functional association of heart rate variability (HRV) with the interaction between three main canonical brain networks in 38 healthy male subjects at rest and directly after a psychosocial stress task. A sliding window approach was used to estimate the functional connectivity (FC) among the salience network (SN), central executive network (CEN), and default mode network (DMN) in 60-s windows on time series of blood-oxygen-level dependent (BOLD) signal. FC between brain networks was calculated by Pearson correlation. A multilevel linear mixed model was conducted to examine the window-by-window association between the root mean square of successive differences between normal heartbeats (RMSSD) and FC of network-pairs across sessions. Our findings showed that the minute-by-minute correlation between the FC and RMSSD was significantly stronger between DMN and CEN than for SN and CEN in the baseline session [b = 4.36, t(5025) = 3.20, p = 0.006]. Additionally, this differential relationship between network pairs and RMSSD disappeared after the stress task; FC between DMN and CEN showed a weaker correlation with RMSSD in comparison to baseline [b = −3.35, t(5025) = −3.47, p = 0.006]. These results suggest a dynamic functional interplay between HRV and the functional association between brain networks that varies depending on the needs created by changing conditions.

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How the brain connects in response to acute stress: A review at the human brain systems level

Cited by 190 publications

References 83 publications

Associations Between Altered Cerebral Activity Patterns and Psychosocial Disorders in Patients With Psychogenic Erectile Dysfunction: A Mediation Analysis of fMRI

Associations Between Altered Cerebral Activity Patterns and Psychosocial Disorders in Patients With Psychogenic Erectile Dysfunction: A Mediation Analysis of fMRI

Rapid Reconfiguration of the Functional Connectome after Chemogenetic Locus Coeruleus Activation

Heart Rate Variability as an Index of Differential Brain Dynamics at Rest and After Acute Stress Induction

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