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

https://doi.org/10.1016/j.neubiorev.2017年10月01日5 Get rights and content

Highlights

  • •
    In health acute stress induces large scale changes at the brain’s network level.
  • •
    The stress response can be described by the dynamical interactions of three networks.
  • •
    The salience and default mode network are both activated by acute stress.
  • •
    Stress may as well improve as deteriorate central executive network functioning.
  • •
    Changes in these three networks account for neuropsychological changes under stress.

Abstract

The brain's response to stress is a matter of extensive neurocognitive research in an attempt to unravel the mechanistic underpinnings of neural adaptation. In line with the broadly defined concept of acute stress, a wide variety of induction procedures are used to mimic stress experimentally. We set out to review commonalities and diversities of the stress-related functional activity and connectivity changes of functional brain networks in healthy adults across procedures. The acute stress response is consistently associated with both increased activity and connectivity in the salience network (SN) and surprisingly also with increased activity in the default mode network (DMN), while most studies show no changes in the central executive network. These results confirm earlier findings of an essential, coordinating role of the SN in the acute stress response and indicate a dynamic role of the DMN whose function is less clear. Moreover, paradigm specific brain responses have to be taken into account when investigating the role and the within and between network connectivity of these three networks.

Introduction

An individual’s ability to cope adaptively with acute stressors is an impressive and important evolutionary capacity (Darwin, 1859). In health, the well-coordinated stress response leads to changes at many levels, including the psychological, behavioral and physiological level. The brain orchestrates this multilevel stress response in order to effectively cope with homeostatic challenges. Both the activated sympathetic adreno-medullary system and the hypothalamus-pituitary-adrenal axis interact at the brain level and function as major effector systems through which the brain influences the body (Ulrich-Lai and Herman, 2009). In health the acute stress response is limited in both duration and amplitude, to ensure that the individual returns to homeostasis during the recovery phase (de Kloet et al., 2005, McEwen and Gianaros, 2011).
Recently, functional brain networks have emerged as the fundamental, organizational elements of human brain architecture. These networks can be identified with functional Magnetic Resonance Imaging (fMRI) both in rest and during a wide variety of tasks, by studying the synchronous (de)activation of brain regions (Beckmann et al., 2005, Laird et al., 2011, Smith et al., 2009). During the acute stress response brain regions do not function in isolation, but are organized into functional networks of dynamically interacting regions, which underscores the need for a systems level neuroscience approach to stress (Bressler, 1995, Hermans et al., 2014). Recent studies have indicated that three of these networks in particular are involved in the acute stress response, i.e. the salience network (SN), the default mode network (DMN) and the central executive network (CEN) (Hermans et al., 2014, Hermans et al., 2011, Qin et al., 2009, Vaisvaser et al., 2013). The so-called triple network model offers a framework for understanding how aberrations in these same networks can lead to a wide range of psychiatric disorders, in which stress also plays an important role (Menon, 2011).
Apart from its adaptive features, the stress response may also contribute to psychopathology (e.g. depression, anxiety and addiction disorders (Faravelli et al., 2012)) when it is inadequate, excessive or prolonged (de Kloet et al., 2005, McEwen and Gianaros, 2011). According to the stress-vulnerability model, the development of psychopathology results from the interaction of certain stressors with specific vulnerabilities of an individual (Faravelli et al., 2012). A better understanding of the stress response in health may ultimately lead to a better understanding of how stress contributes to psychopathology in vulnerable individuals.
For research purposes, stress has been experimentally induced in healthy subjects by a variety of psychological and physical stressors of which some can also be used during MRI scanning. Commonly used experimental stress paradigms in the scanner range from social evaluative stress to watching aversive movies or experiencing excessive cold (Bali and Jaggi, 2015). These paradigms often involve different conditions and tasks that have to be performed. We propose that these different paradigms lead to distinct, specific brain effects that are related to the methods used (Hermans et al., 2011, Koric et al., 2012, Seo et al., 2011), which should be dissociated from more general patterns, that may point towards common activity and connectivity patterns in acute stress (Hermans et al., 2014).
Here we will review the fMRI studies that compare the brain’s stress response to the non-stressed brain in healthy subjects, from the triple network perspective. While Hermans et al. (2014) describe the role of the SN and CEN in the acute stress response in their qualitative review, we now aim to systematically review the fMRI studies on acute stress. In this review we will not only focus on the SN and CEN, but also include the DMN, since we think that the acute stress response can best be characterized by describing the changes in these three networks. Both activity and connectivity studies are included, which give complementary information and together offer a fuller scope of the brain’s stress response. We start with giving a short overview of the methods for stress induction in the MRI environment and introduce the networks under study. Subsequently, we provide a critical appraisal of the available studies on the brain’s stress response and the recovery from stress. Finally, we integrate the results into a network perspective of the stress response.

Section snippets

Stress induction methods

In accordance with a previous review on stress induction methods (Bali and Jaggi, 2015), we include both physical (physiological and/or environmental) and psychological methods. The physical methods directly induce physiological changes, while psychological methods induce stress without directly affecting the body. The psychological methods included in this review induce stress by either a combination of a higher-order cognitive task with social evaluative stress or by confronting the subject

Core large-scale networks under study

Advances in network-based research in neuroscience made it possible to identify functional networks, which consist of interconnected brain areas that are distributed across the brain. An important methodological development was the finding that these networks can consistently be identified during the ‘resting-state’, i.e. when a subject is not engaged in any particular task (Beckmann et al., 2005, Biswal et al., 1995). Later it was shown that these networks can also be identified during a wide

fMRI analysis methods

In this review we address the effects of stress on functional MRI activity and connectivity in the brain. Activity studies investigate differences in the amount of blood-oxygen-level-dependent (BOLD) signal by contrasting different conditions, while connectivity studies investigate patterns of synchronized activity between different brain regions. Connectivity can be measured during a task, but also when a subject is not engaged in any particular task, which is called resting state functional

Literature search

A search was performed in Pubmed/Medline, Embase and PsycINFO to identify articles in English, reporting on functional connectivity and activity changes in the brain in response to acute stress induction. The following search terms and their synonyms were used: "stress", "functional connectivity", "fMRI", and "healthy". Additionally, the names of the different stress induction methods were added to the search (see Appendix A for the complete search). Studies were selected if they 1) included

Search results

The search yielded 3690 articles, with 1391 articles in Pubmed/Medline, 1617 articles in EMBASE and 682 articles in PsycINFO (see flowchart in Fig. 2). Deduplication resulted in 2253 articles. After screening title and abstract, fifty-six articles were selected for reading the full text, after which twenty-nine articles were included. Common reasons for exclusion were 1) the use of other imaging techniques than MRI, 2) the stress response was not compared to a non-stress control condition or 3)

Discussion

The aim of this study was to review the literature on the brain response to acute stress in healthy, adult subjects and integrate the results within a network perspective. Following our earlier line of thought we focus on the SN, DMN and CEN. We start with discussing the quality of the available evidence, followed by describing the findings for the networks under study. Finally, we will try to integrate the results into a network perspective on the stress response.

Declaration of interest

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors and the authors declare to have no conflicts of interest related to this study.

References (91)

  • J.P. Hamilton et al.

    Default-mode and task-positive network activity in major depressive disorder: implications for adaptive and maladaptive rumination

    Biol. Psychiatry

    (2011)
  • E.J. Hermans et al.

    Dynamic adaptation of large-scale brain networks in response to acute stressors

    Trends Neurosci.

    (2014)
  • P. Kumar et al.

    Differential effects of acute stress on anticipatory and consummatory phases of reward processing

    Neuroscience

    (2014)
  • V. Menon

    Large-scale brain networks and psychopathology: a unifying triple network model

    Trends Cogn. Sci.

    (2011)
  • P.C. Mulders et al.

    Resting-state functional connectivity in major depressive disorder: a review

    Neurosci. Biobehav. Rev.

    (2015)
  • K.a. Muscatell et al.

    Greater amygdala activity and dorsomedial prefrontal-amygdala coupling are associated with enhanced inflammatory responses to stress

    Brain. Behav. Immun.

    (2015)
  • N.Y.L. Oei et al.

    Acute stress-induced cortisol elevations mediate reward system activity during subconscious processing of sexual stimuli

    Psychoneuroendocrinology

    (2014)
  • L. Ossewaarde et al.

    Neural mechanisms underlying changes in stress-sensitivity across the menstrual cycle

    Psychoneuroendocrinology

    (2010)
  • L. Ossewaarde et al.

    Stress-induced reduction in reward-related prefrontal cortex function

    Neuroimage

    (2011)
  • A.J. Porcelli et al.

    The effects of acute stress on human prefrontal working memory systems

    Physiol. Behav.

    (2008)
  • J.C. Pruessner et al.

    Deactivation of the limbic system during acute psychosocial stress: evidence from positron emission tomography and functional magnetic resonance imaging studies

    Biol. Psychiatry

    (2008)
  • S. Qin et al.

    Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex

    Biol. Psychiatry

    (2009)
  • M.A. Rogers et al.

    Executive and prefrontal dysfunction in unipolar depression: a review of neuropsychological and imaging evidence

    Neurosci. Res.

    (2004)
  • H.J.F.F. van Marle et al.

    From specificity to sensitivity: how acute stress affects amygdala processing of biologically salient stimuli

    Biol. Psychiatry

    (2009)
  • H.J.F. van Marle et al.

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

    Neuroimage

    (2010)
  • I.M. Veer et al.

    Beyond acute social stress: increased functional connectivity between amygdala and cortical midline structures

    Neuroimage

    (2011)
  • J. Wagner et al.

    Feasibility of testing three salivary stress biomarkers in relation to naturalistic traffic noise exposure

    Int. J. Hyg. Environ. Health

    (2010)
  • P. Yilmaz et al.

    Brain correlates of stress-induced analgesia

    Pain

    (2010)
  • Y. Zhou et al.

    Increased neural resources recruitment in the intrinsic organization in major depression

    J. Affect. Disord.

    (2010)
  • C. Akdeniz et al.

    Neuroimaging evidence for a role of neural social stress processing in ethnic minority–associated environmental risk

    JAMA Psychiatry

    (2014)
  • J.R. Andrews-Hanna et al.

    The default network and self-generated thought: component processes, dynamic control, and clinical relevance

    Ann. N. Y. Acad. Sci.

    (2014)
  • A.F.T. Arnsten

    Stress signalling pathways that impair prefrontal cortex structure and function

    Nat. Rev. Neurosci.

    (2009)
  • A. Bali et al.

    Clinical experimental stress studies: methods and assessment

    Rev. Neurosci.

    (2015)
  • C.F. Beckmann et al.

    Investigations into resting-state connectivity using independent component analysis

    Philos. Trans. R. Soc. B

    (2005)
  • S. Bendahan et al.

    Acute stress alters individual risk taking in a time- dependent manner and leads to anti-social risk

    Eur. J. Neurosci.

    (2017)
  • B. Biswal et al.

    Functional connectivity in the motor cortex of resting human brain using echo-planar mri

    Magn. Reson. Med.

    (1995)
  • A. Boehringer et al.

    Neural correlates of the cortisol awakening response in humans

    Neuropsychopharmacology

    (2015)
  • R.L. Buckner et al.

    The brain’s default network: anatomy, function, and relevance to disease

    Ann. N. Y. Acad. Sci.

    (2008)
  • A.E. Cavanna et al.

    The precuneus: a review of its functional anatomy and behavioural correlates

    Brain

    (2006)
  • M. Corbetta et al.

    Control of goal-directed and stimulus-driven attention in the brain

    Nat. Rev. Neurosci.

    (2002)
  • N.S. Corral-Frías et al.

    Stress-related anhedonia is associated with ventral striatum reactivity to reward and transdiagnostic psychiatric symptomatology

    Psychol. Med.

    (2015)
  • B.N. Cuthbert

    The RDoC framework: facilitating transition from ICD/DSM to dimensional approaches that integrate neuroscience and psychopathology

    World Psychiatry

    (2014)
  • J.S. Damoiseaux et al.

    Consistent Resting-State Networks

    (2006)
  • C. Darwin

    On the Origin of Species by Means of Natural Selection

    (1859)
  • E.R. de Kloet et al.

    Stress and the brain: from adaptation to disease

    Nat. Rev. Neurosci.

    (2005)

    • Cited by (181)

    View all citing articles on Scopus
    View full text
    © 2017 Elsevier Ltd. All rights reserved.