Autonomic regulation and vagal tone

Autonomy of autonomic dysfunction in major depression.: Objective: To investigate cardiac autonomic dysfunction in patients with major depressive disorder (MDD). Research in this area has faced several limitations because of the heterogeneity of the disease, the influence of medication, and methodological shortcomings. Methods: Participants were 75 patients suffering from an acute recurrent episode of MDD and 75 matched controls. All participants were assessed at baseline for linear and nonlinear parameters of heart rate variability, QT variability a

Non-invasive vagus nerve stimulation acutely improves spontaneous cardiac baroreflex sensitivity in healthy young men: A randomized placebo-controlled trial.: Background: Despite positive outcomes of transcutaneous vagus nerve stimulation (tVNS) via the auricular branch of the vagus nerve (ABVN), the mechanisms underlying these outcomes remain unclear. Additionally, previous studies have not been controlled the possible placebo effects of tVNS. Objective: To test the hypothesis that tVNS acutely improves spontaneous cardiac baroreflex sensitivity (cBRS) and autonomic modulation, and that these effects are specific to stimulation of ABVN. Methods: Thir

Non-invasive vagus nerve stimulation in healthy humans reduces sympathetic nerve activity.: Background: Vagus nerve stimulation (VNS) is currently used to treat refractory epilepsy and is being investigated as a potential therapy for a range of conditions, including heart failure, tinnitus, obesity and Alzheimer's disease. However, the invasive nature and expense limits the use of VNS in patient populations and hinders the exploration of the mechanisms involved. Objective: We investigated a non-invasive method of VNS through electrical stimulation of the auricular branch of the vagus n

Effects of transcutaneous vagus nerve stimulation in individuals aged 55 years or above: potential benefits of daily stimulation.: Ageing is associated with attenuated autonomic function. Transcutaneous vagal nerve stimulation (tVNS) improved autonomic function in healthy young participants. We therefore investigated the effects of a single session of tVNS (studies 1 and 2) and tVNS administered daily for two weeks (study 3) in volunteers aged ≥ 55 years. tVNS was performed using modified surface electrodes on the tragus and connected to a transcutaneous electrical nerve stimulation (TENS) machine. Study 1: participants (n=

Modulation of vagal tone enhances gastroduodenal motility and reduces somatic pain sensitivity.: Background: The parasympathetic nervous system, whose main neural substrate is the vagus nerve, exerts a fundamental antinociceptive role and influences gastrointestinal sensori-motor function. Our research question was to whether combined electrical and physiological modulation of vagal tone, using transcutaneous electrical vagal nerve stimulation (t-VNS) and deep slow breathing (DSB) respectively, could increase musculoskeletal pain thresholds and enhance gastroduodenal motility in healthy sub

Sex differences in healthy human heart rate variability: A meta-analysis.: The present meta-analysis aimed to quantify current evidence on sex differences in the autonomic control of the heart, indexed by measures of heart rate variability (HRV) in healthy human subjects. An extensive search of the literature yielded 2020 titles and abstracts, of which 172 provided sufficient reporting of sex difference in HRV. Data from 63,612 participants (31,970 females) were available for analysis. Meta-analysis yielded a total of 1154 effect size estimates (k) across 50 different

Heart rate variability mediates the link between rumination and depressive symptoms: A longitudinal study.

Ruminative thinking about negative feelings has been prospectively associated with increases in depressive symptoms and heightened risk for new onsets of major depression. One putative pathophysiological mechanism underlying this link might be represented by autonomic nervous system dysfunction. The objective of this longitudinal study was to evaluate the interplay between rumination, autonomic function (as revealed by heart rate variability (HRV) analysis), and depressive symptoms in healthy young subjects, over a three-year period. Rumination and depressive symptoms were evaluated in twenty-two women and twenty men at three assessment points (Time 0, 1 and 2) by the score on the Ruminative Response Scale, and the Center for Epidemiological Studies Depression Scale, respectively. Vagally-mediated HRV was assessed in a laboratory session (Time 0) and in two ambulatory sessions at Time 1 …

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Emotional orienting during interoceptive threat in orthostatic intolerance: Dysautonomic contributions to psychological symptomatology in the postural tachycardia syndrome and vasovagal syncope.

Cognitive and emotional processes are influenced by interoception (homeostatic somatic feedback), particularly when physiological arousal is unexpected and discrepancies between predicted and experienced interoceptive signals may engender anxiety. Due to the vulnerability for comorbid psychological symptoms in forms of orthostatic intolerance (OI), this study investigated psychophysiological contributions to emotional symptomatology in 20 healthy control participants (13 females, mean age 36 ± 8 years), 20 postural tachycardia syndrome (PoTS) patients (18 females, mean age 38 ± 13 years) and 20 vasovagal syncope (VVS) patients (15 females, mean age 39 ± 12 years). We investigated indices of emotional orienting responses (OR) to randomly presented neutral, pleasant and unpleasant images in the supine position and during the induced interoceptive threat of symptom provocation of head-up ti…

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Circadian variation of heart rate variability across sleep stages.

Study objectives: Nocturnal cardiovascular events are more frequent at the beginning and end of the night. It was proposed that this pattern reflects the nocturnal distribution of sleep and sleep stages. Using heart rate variability (HRV), we recently showed an interaction between the circadian system and vigilance states on the regulation of cardiac rhythmicity. Here, we further investigate this interaction in order to clarify the specific effects of sleep stages on the regulation of the heart. Design: Participants underwent a 72-h ultradian sleep-wake cycle procedure in time isolation consisting of alternating 60-min wake episodes in dim light and 60-min nap opportunities in total darkness. Setting: Time isolation suite. Patients or participants: Fifteen healthy young participants; two were subsequently excluded. Interventions: N/A. Measurements and results: The current study revealed …

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Autonomic and prefrontal events during moral elevation.

Moral elevation, or elevation, is a specific emotional state triggered by witnessing displays of profound virtue and moral beauty. This study set out to characterize the physiology underlying elevation with measurements of heart rate (HR), respiratory sinus arrhythmia (RSA), and medial prefrontal cortex (mPFC) activity. During elevation, HR and RSA increased. These findings illustrate that elevation involves an uncommon combination of both sympathetic and parasympathetic activation, which is present in circumstances where arousal and social engagement are both required. In addition, we show evidence of content-dependent alterations of mPFC activity during elevation peaks. Altogether, this study shows that the induction of moral elevation recruits an uncommon autonomic and neural pattern that is consistent with previous understanding of socioemotional-induced allostasis.

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Increased sympathetic and decreased parasympathetic activity rather than changes in hypothalamic-pituitary-adrenal axis activity is associated with metabolic abnormalities.

Context: Stress is suggested to lead to metabolic dysregulations as clustered in the metabolic syndrome, but the underlying biological mechanisms are not yet well understood. Objective: We examined the relationship between two main str systems, the autonomic nervous system and the hypothalamic-pituitary-adrenal (HPA) axis, with the metabolic syndrome and its components. Design: The design was baseline data (yr 2004-2007) of a prospective cohort: the Netherlands Study of Depression and Anxiety (NESDA). Setting: The study comprised general community, primary care, and specialized mental health care. Participants: This study included 1883 participants aged 18-65 yr. Main outcome measures: Autonomic nervous system measures included heart rate, respiratory sinus arrhythmia (RSA; high RSA reflecting high parasympathetic activity), and preejection period (PEP; high PEP reflecting low sympatheti…

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Short-term autonomic and cardiovascular effects of mindfulness body scan meditation.

Background: Recent research suggests that the Mindfulness-Based Stress Reduction program has positive effects on health, but little is known about the immediate physiological effects of different components of the program. Purpose: To examine the short-term autonomic and cardiovascular effects of one of the techniques employed in mindfulness meditation training, a basic body scan meditation. Methods: In Study 1, 32 healthy young adults (23 women, 9 men) were assigned randomly to either a meditation, progressive muscular relaxation or wait-list control group. Each participated in two laboratory sessions 4 weeks apart in which they practiced their assigned technique. In Study 2, using a within-subjects design, 30 healthy young adults (15 women, 15 men) participated in two laboratory sessions in which they practiced meditation or listened to an audiotape of a popular novel in counterbalance…

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Association between major depressive disorder and heart rate variability in the Netherlands Study of Depression and Anxiety (NESDA).

Context: It has been hypothesized that depression is associated with lower heart rate variability and decreased cardiac vagal control. This may play an important role in the risk of cardiovascular disease among depressed individuals. Objective: To determine whether heart rate variability was lower in depressed individuals than in healthy controls in a large adult sample. Design: Cross-sectional analyses from a large depression cohort study. Setting: The Netherlands Study of Depression and Anxiety. Participants: Two thousand three hundred seventy-three individuals (mean age, 41.8 years; 66.8% female) who participated in the Netherlands Study of Depression and Anxiety. Included were 524 controls, 774 individuals with a diagnosis of major depressive disorder (MDD) earlier in life (remitted MDD), and 1075 individuals with current MDD based on the Composite International Diagnostic Interview.…

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Fatigue following COVID-19 infection is not associated with autonomic dysfunction.

Background: The long-term clinical and physiological consequences of COVID-19 infection remain unclear. While fatigue has emerged as a common symptom following infection, little is known about its links with autonomic dysfunction. SARS-CoV-2 is known to infect endothelial cells in acute infection, resulting in autonomic dysfunction. Here we set out to test the hypothesis that this results in persistent autonomic dysfunction and is associated with post-COVID fatigue in convalescent patients. Methods: We recruited 20 fatigued and 20 non-fatigued post-COVID patients (median age 44.5 years, 36/40 (90%) female, median time to follow up 166.5 days). Fatigue was assessed using the Chalder Fatigue Scale. These underwent the Ewing's autonomic function test battery, including deep breathing, active standing, Valsalva manoeuvre and cold-pressor testing, with continuous electrocardiogram and blood p…

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Cold pressor stress induces opposite effects on cardioceptive accuracy dependent on assessment paradigm.

Interoception depends on visceral afferent neurotraffic and central control processes. Physiological arousal and organ activation provide the biochemical and mechanical basis for visceral afferent neurotraffic. Perception of visceral symptoms occurs when attention is directed toward body sensations. Clinical studies suggest that stress contributes to the generation of visceral symptoms. However, during stress exposure attention is normally shifted away from bodily signals. Therefore, the net effects of stress on interoception remain unclear. We, therefore, investigated the impact of the cold pressor test or a control intervention (each n=21) on three established laboratory paradigms to assess cardioceptive accuracy (CA): for the Schandry-paradigm, participants were asked to count heartbeats, while during the Whitehead-tasks subjects were asked to rate whether a cardiac sensation appeared…

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Effects of short-term food deprivation on interoceptive awareness, feelings and autonomic cardiac activity.

The perception of internal bodily signals (interoception) plays a relevant role for emotion processing and feelings. This study investigated changes of interoceptive awareness and cardiac autonomic activity induced by short-term food deprivation and its relationship to hunger and affective experience. 20 healthy women were exposed to 24h of food deprivation in a controlled setting. Interoceptive awareness was assessed by using a heartbeat tracking task. Felt hunger, cardiac autonomic activity, mood and subjective appraisal of interoceptive sensations were assessed before and after fasting. Results show that short-term fasting intensifies interoceptive awareness, not restricted to food cues, via changes of autonomic cardiac and/or cardiodynamic activity. The increase of interoceptive awareness was positively related to felt hunger. Additionally, the results demonstrate the role of cardiac…

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Continuous low-level vagus nerve stimulation reduces stellate ganglion nerve activity and paroxysmal atrial tachyarrhythmias in ambulatory canines.

Background: We hypothesize that left-sided low-level vagus nerve stimulation (LL-VNS) can suppress sympathetic outflow and reduce atrial tachyarrhythmias in ambulatory dogs. Methods and results: We implanted a neurostimulator in 12 dogs to stimulate the left cervical vagus nerve and a radiotransmitter for continuous recording of left stellate ganglion nerve activity, vagal nerve activities, and ECGs. Group 1 dogs (N=6) underwent 1 week of continuous LL-VNS. Group 2 dogs (N=6) underwent intermittent rapid atrial pacing followed by active or sham LL-VNS on alternate weeks. Integrated stellate ganglion nerve activity was significantly reduced during LL-VNS (7.8 mV/s; 95% confidence interval [CI] 6.94 to 8.66 versus 9.4 mV/s [95% CI, 8.5 to 10.3] at baseline; P=0.033) in group 1. The reduction was most apparent at 8 am, along with a significantly reduced heart rate (P=0.008). Left-sided low-…

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Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation.

Positive social interactions and social support may protect against various forms of mental and physical illness, although the mechanisms for these effects are not well identified. The socially monogamous prairie vole, which--like humans--forms social bonds and displays high levels of parasympathetic activity, has provided a useful model for investigating neurobiological systems that mediate the consequences of sociality. In the present study, adult female prairie voles were exposed to social isolation or continued pairing with a female sibling (control conditions) for 4 weeks. During weeks 3 and 4 of this period, animals were administered oxytocin (20 microg/50 microl, s.c.) or saline vehicle (50 microl, s.c.) daily for a total of 14 days. In Experiment 1, autonomic parameters were recorded during and following isolation or pairing. Isolation (vs. pairing) significantly increased basal …

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Parasympathetic and sympathetic responses to the strange situation in infants and mothers from avoidant and securely attached dyads.

Vagal reactivity and salivary alpha-amylase (sAA) were assessed in infants (M age = 13.55 months) and their mothers during the Strange Situation Paradigm (SSP) to investigate differences in physiological responses in a sample of insecure-avoidant and securely-attached dyads (N = 132). Infants classified as insecure-avoidant had significantly higher vagal withdrawal during the SSP and higher sAA overall, suggesting that the avoidant attachment pattern is associated with a greater allostatic load. During separation episodes of the SSP, all mothers showed significant vagal withdrawal, suggesting greater attempts at regulation. During the last reunion, typically the most stressful episode for infants, mothers of secure infants showed greater vagal withdrawal than mothers of insecure-avoidant infants, suggesting greater attempts by these mothers at interactive repair. Results for mothers and …

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BOLD fMRI deactivation of limbic and temporal brain structures and mood enhancing effect by transcutaneous vagus nerve stimulation.

Unlabelled: Direct vagus nerve stimulation (VNS) has proved to be an effective treatment for seizure disorder and major depression. However, since this invasive technique implies surgery, with its side-effects and relatively high financial costs, a non-invasive method to stimulate vagal afferences would be a great step forward. We studied effects of non-invasive electrical stimulation of the nerves in the left outer auditory canal in healthy subjects (n = 22), aiming to activate vagal afferences transcutaneously (t-VNS). Short-term changes in brain activation and subjective well-being induced by t-VNS were investigated by functional magnetic resonance imaging (fMRI) and psychometric assessment using the Adjective Mood Scale (AMS), a self-rating scale for current subjective feeling. Stimulation of the ear lobe served as a sham control. fMRI showed that robust t-VNS induced BOLD-signal dec…

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Interoceptive rhythms in the brain.

Sensing internal bodily signals, or interoception, is fundamental to maintain life. However, interoception should not be viewed as an isolated domain, as it interacts with exteroception, cognition and action to ensure the integrity of the organism. Focusing on cardiac, respiratory and gastric rhythms, we review evidence that interoception is anatomically and functionally intertwined with the processing of signals from the external environment. Interactions arise at all stages, from the peripheral transduction of interoceptive signals to sensory processing and cortical integration, in a network that extends beyond core interoceptive regions. Interoceptive rhythms contribute to functions ranging from perceptual detection up to sense of self, or conversely compete with external inputs. Renewed interest in interoception revives long-standing issues on how the brain integrates and coordinates…

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The Fundamental Basis of Palpitations: A Neurocardiology Approach.

Background and objective: Palpitations are a common symptom that may indicate cardiac arrhythmias, be a somatic complaint in anxiety disorders, and can be present in patients without either condition. The objective of this review was to explore the pathways and fundamental mechanisms through which individuals appreciate palpitations. Observations: Cardiac afferents provide beat-to-beat sensory information on the heart to the spinal cord, brain stem, and higher brain centers. Cardioception, a subset of interoception ('the physiological sense of the condition of the body'), refers to sensing of the heartbeat. High cardioception is present in persons with lower body mass index, lower percentages of body fat, and anxiety disorders. Low cardioception (lower interoceptive awareness) is associated with psychiatric disorders, such as depression, personality disorders, and schizophrenia. CNS site…

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Atypical interoception as a common risk factor for psychopathology: A review.

The inadequacy of a categorial approach to mental health diagnosis is now well-recognised, with many authors, diagnostic manuals and funding bodies advocating a dimensional, trans-diagnostic approach to mental health research. Variance in interoception, the ability to perceive one's internal bodily state, is reported across diagnostic boundaries, and is associated with atypical functioning across symptom categories. Drawing on behavioural and neuroscientific evidence, we outline current research on the contribution of interoception to numerous cognitive and affective abilities (in both typical and clinical populations), and describe the interoceptive atypicalities seen in a range of psychiatric conditions. We discuss the role that interoception may play in the development and maintenance of psychopathology, as well as the ways in which interoception may differ across clinical presentatio…

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Interoception and psychopathology: A developmental neuroscience perspective.

Interoception refers to the perception of the physiological condition of the body, including hunger, temperature, and heart rate. There is a growing appreciation that interoception is integral to higher-order cognition. Indeed, existing research indicates an association between low interoceptive sensitivity and alexithymia (a difficulty identifying one's own emotion), underscoring the link between bodily and emotional awareness. Despite this appreciation, the developmental trajectory of interoception across the lifespan remains under-researched, with clear gaps in our understanding. This qualitative review and opinion paper provides a brief overview of interoception, discussing its relevance for developmental psychopathology, and highlighting measurement issues, before surveying the available work on interoception across four stages of development: infancy, childhood, adolescence and lat…

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Towards a psychophysics of interoceptive processes: the measurement of heartbeat detection.

It is difficult to collect objective evidence of interoception. Unlike exteroception, the effective stimuli for interoception are often unknown, and even when identifiable, they are difficult to control experimentally. Furthermore, direct stimulation of the interoceptors is seldom appropriate in human experimentation. Hence, non-invasive behavioural measures of accuracy in heartbeat detection have frequently been adopted to index interoceptive sensitivity. However, there has been little standardization and the two most popular methods for assessing heartbeat detection, heartbeat tracking and two alternative forced choice methods, appear to be biased and of questionable validity. These issues do not arise with other methods that are based on classical psychophysics and that enable subjects to indicate when during the cardiac cycle their heartbeat sensations occur. Not only are these class…

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Technical and clinical aspects of cortisol as a biochemical marker of chronic stress.

Stress is now recognized as a universal premorbid factor associated with many risk factors of various chronic diseases. Acute stress may induce an individual's adaptive response to environmental demands. However, chronic, excessive stress causes cumulative negative impacts on health outcomes through "allostatic load". Thus, monitoring the quantified levels of long-term stress mediators would provide a timely opportunity for prevention or earlier intervention of stress-related chronic illnesses. Although either acute or chronic stress could be quantified through measurement of changes in physiological parameters such as heart rate, blood pressure, and levels of various metabolic hormones, it is still elusive to interpret whether the changes in circulating levels of stress mediators such as cortisol can reflect the acute, chronic, or diurnal variations. Both serum and salivary cortisol lev…

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Interoceptive sensitivity in anxiety and anxiety disorders: an overview and integration of neurobiological findings.

Interoceptive sensitivity, particularly regarding heartbeat, has been suggested to play a pivotal role in the pathogenesis of anxiety and anxiety disorders. This review provides an overview of methods which are frequently used to assess heartbeat perception in clinical studies and summarizes presently available results referring to interoceptive sensitivity with respect to heartbeat in anxiety-related traits (anxiety sensitivity, state/trait anxiety), panic disorder and other anxiety disorders. In addition, recent neurobiological studies of neuronal activation correlates of heartbeat perception using positron emission tomography (PET), functional magnetic resonance imaging (fMRI) or electroencephalographic (EEG) techniques are presented. Finally, possible clinical and therapeutic implications (e.g., beta-blockers, biofeedback therapy, cognitive interventions and interoceptive exposure) o…

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New aspects of oxytocin receptor function revealed by knockout mice: sociosexual behaviour and control of energy balance.

To further define the function of the oxytocin receptor (OXTR) in vivo, we generated mice deficient in the Oxtr gene (Oxtr-/-). Oxtr-/- mice had no obvious deficits in fertility or sexual behaviour, but displayed several aberrations in social behaviours, including male aggression, and mother-offspring interaction. In addition, they showed novel physiological defects including obesity, and dysfunction in body temperature control when exposed to cold. We review here our new findings with Oxtr-/- mice, and introduce newly generated Oxtr-Venus knockin mice as a potential tool for examining molecular physiology of Oxtr-neurons.

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Chronic psychosocial factors and acute physiological responses to laboratory-induced stress in healthy populations: a quantitative review of 30 years of investigations.

This meta-analysis included 729 studies from 161 articles investigating how acute stress responsivity (including stress reactivity and recovery of hypothalamic-pituitary-adrenal [HPA] axis, autonomic, and cardiovascular systems) changes with various chronic psychosocial exposures (job stress; general life stress; depression or hopelessness; anxiety, neuroticism, or negative affect; hostility, aggression, or Type-A behavior; fatigue, burnout, or exhaustion; positive psychological states or traits) in healthy populations. In either the overall meta-analysis or the methodologically strong subanalysis, positive psychological states or traits were associated with reduced HPA reactivity. Hostility, aggression, or Type-A behavior was associated with increased cardiovascular (heart rate or blood pressure) reactivity, whereas anxiety, neuroticism, or negative affect was associated with decreased …

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Transcutaneous vagus nerve stimulation reduces serum high mobility group box 1 levels and improves survival in murine sepsis.

Objective: Electrical vagus nerve stimulation inhibits proinflammatory cytokine production and prevents shock during lethal systemic inflammation through an alpha7 nicotinic acetylcholine receptor (alpha7nAChR)-dependent pathway to the spleen, termed the cholinergic anti-inflammatory pathway. Pharmacologic alpha7nAChR agonists inhibit production of the critical proinflammatory mediator high mobility group box 1 (HMGB1) and rescue mice from lethal polymicrobial sepsis. Here we developed a method of transcutaneous mechanical vagus nerve stimulation and then investigated whether this therapy can protect mice against sepsis lethality. Design: Prospective, randomized study. Setting: Institute-based research laboratory. Subjects: Male BALB/c mice. Interventions: Mice received lipopolysaccharide to induce lethal endotoxemia or underwent cecal ligation and puncture to induce polymicrobial sepsis…

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Brain-gut-microbiota axis in depression: A historical overview and future directions.

Depression is the most common mental disorder and a leading cause of disability worldwide. Despite abundant research, the precise mechanisms underlying the pathophysiology of depression remain elusive. Accumulating evidence from preclinical and clinical studies suggests that alterations in the gut microbiota, microbe-derived short-chain fatty acids, D-amino acids and metabolites play a key role in the pathophysiology of depression via the brain-gut-microbiota axis, including the neural and immune systems. Notably, the brain-gut-microbiota axis might play a crucial role in susceptibility versus resilience in rodents exposed to stress. Vagotomy is reported to block depression-like phenotypes in rodents after fecal microbiota transplantation of "depression-related" microbiome, suggesting that the vagus nerve influences depression through the brain-gut-microbiota axis. In this article, we re…

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