Publications by authors named "Luca Carnevali"

48 Publications

Reduced recognition of facial emotional expressions in global burnout and burnout depersonalization in healthcare providers.

PeerJ 2021 13;9:e10610. Epub 2021 Jan 13.

Department of Experimental, Diagnostic and Specialty Medicine, University of Bologna, Bologna, Italy.

The healthcare provider profession strongly relies on the ability to care for others' emotional experiences. To what extent burnout may relate to an actual alteration of this key professional ability has been little investigated. In an experimentally controlled setting, we investigated whether subjective experiences of global burnout or burnout depersonalization (the interpersonal component of burnout) relate to objectively measured alterations in emotion recognition and to what extent such alterations are emotion specific. Healthcare workers ( = 90) completed the Maslach Burnout Inventory and a dynamic emotion recognition task in which faces with neutral emotional expressions gradually changed to display a specific basic emotion (happiness, anger, fear, or sadness). Participants were asked to identify and then classify each displayed emotion. Before the task, a subsample of 46 participants underwent two salivary cortisol assessments. Individuals with global burnout were less accurate at recognizing others' emotional expressions of anger and fear, tending to misclassify these as happiness, compared to individuals without global burnout. Individuals with high burnout depersonalization were more accurate in recognizing happiness and less accurate in recognizing all negative emotions, with a tendency to misclassify the latter as positive ones, compared to healthcare workers with moderate/low depersonalization. Moreover, individuals with high depersonalization-but not participants with global burnout-were characterized by higher cortisol levels. These results suggest that the subjective burnout experience relates to an actual, but selective, reduction in the recognition of facial emotional expressions, characterized by a tendency to misclassify negative emotional expressions as positive ones, perhaps due to an enhanced seeking of positive social cues. This study adds to the understanding of emotional processing in burnout and paves the way for more nuanced studies on the role of altered processing of threat signals in the development and/or persistence of burnout.
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http://dx.doi.org/10.7717/peerj.10610DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7811292PMC
January 2021

Osteopathic Manipulative Treatment and Cardiovascular Autonomic Parameters in Rugby Players: A Randomized, Sham-Controlled Trial.

J Manipulative Physiol Ther 2021 Jan 9. Epub 2021 Jan 9.

Stress Physiology Lab, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy; Stress Control Lab, Collegio Italiano di Osteopatia, Parma, Italy.

Objective: The purpose of this study was to investigate the effects of osteopathic manipulative treatment (OMT) on cardiovascular autonomic parameters after a rugby match.

Methods: Resting and reactivity (ie, response to orthostasis) measures of mean arterial pressure, heart rate, and heart rate variability were assessed in 23 male players after a single session of OMT, both 18 to 20 hours after a rugby match and in a corresponding no-match condition, in a randomized, sham-controlled, crossover design.

Results: Signs of reduced heart rate variability and elevated mean arterial pressure and heart rate were found 18 to 20 hours after a rugby match compared with the no-match condition. A significant increase in heart rate variability and a significant reduction in mean arterial pressure were observed after OMT in both the after-match and no-match conditions. Heart rate and heart rate variability responses to orthostasis were not affected by previous match competition, but were significantly larger after OMT compared with sham treatment.

Conclusion: This study suggests the presence of cardiovascular autonomic alterations in rugby players after a competitive match, which may be indicative of prolonged fatigue and incomplete recovery. In these players, favorable changes in cardiovascular autonomic parameters were observed following a single session of OMT.
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http://dx.doi.org/10.1016/j.jmpt.2020.09.002DOI Listing
January 2021

Angry in America: Psychophysiological Responses to Unfair Treatment.

Ann Behav Med 2020 12;54(12):924-931

Department of Psychological Science, University of California, Irvine, CA, USA.

Background: African Americans have the highest rates of hypertension-related disease of any ethnic group in the USA. Importantly, racism and discrimination have been linked to these higher rates of morbidity and mortality. Discrimination is deleterious not only to those that are the recipients of this unfair treatment but also to the partners and family members of those affected as well to those that perpetrate this bias.

Purpose: In this paper, we identify a unique pattern of physiological response to unfair treatment, we have called the "cardiovascular conundrum." This pattern is characterized by greater heart rate variability and greater total peripheral resistance in African Americans compared to their European American counterparts.

Methods And Results: We review the evidence supporting the existence of this pattern and propose several physiological and psychological factors that might underpin it. We also propose a number of factors that might help to mitigate the deleterious effects associated with it.

Conclusions: Whereas the context of the current review is on Black/White disparities the framework we propose may be relevant to others exposed to unfair treatment. Ultimately, the systemic factors that perpetuate these inequalities will require that we first acknowledge and then face the challenges they present if we are to address the wealth and health disparities in our country.
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http://dx.doi.org/10.1093/abm/kaaa094DOI Listing
December 2020

Dissociating cognitive, behavioral and physiological stress-related responses through dorsolateral prefrontal cortex inhibition.

Psychoneuroendocrinology 2021 Feb 1;124:105070. Epub 2020 Dec 1.

Department of Psychology, Sapienza University of Rome, Rome, Italy; IRCCS Santa Lucia Foundation, Rome, Italy. Electronic address:

The left dorsolateral prefrontal cortex (dlPFC) has been implicated in the regulation of stress-related cognitive processes and physiological responses and is the principal target of noninvasive brain stimulation techniques applied to psychiatric conditions. However, existing studies are mostly correlational and causal evidence on the role of this region in mediating specific psychophysiological mechanisms underpinning stress-related responses are needed to make the application of such techniques more efficient. To fill this gap, this study used inhibitory continuous theta burst stimulation (cTBS) in healthy individuals to examine the extent to which activity of the left dlPFC is associated with cognitive (subjective focus on a tracking task), behavioral (reaction times and variability), and physiological responses (heart rate and its variability and cortisol level) following induction of perseverative cognition. Compared to sham and left ventral PreMotor area stimulation (as active control area), inhibition of left dlPFC determined sustained autonomic and neuroendocrine activation and increased the subjective perception of being task-focused, while not changing the behavioral and self-reported stress-related responses. Adopting a causative approach, we describe a role of left dlPFC in inhibitory control of the physiological stress-response associated to perseverative thinking.
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http://dx.doi.org/10.1016/j.psyneuen.2020.105070DOI Listing
February 2021

Exploring the Effects of Osteopathic Manipulative Treatment on Autonomic Function Through the Lens of Heart Rate Variability.

Front Neurosci 2020 7;14:579365. Epub 2020 Oct 7.

Stress Physiology Lab, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy.

The osteopathic community has long hypothesized that the autonomic nervous system (ANS) represents one of the putative substrates through which osteopathic manipulative treatment (OMT) can improve body functions that have been altered by musculoskeletal alterations. Heart rate variability (HRV) is an important physiological measure of cardiac ANS activity. Emerging evidence suggests that OMT is associated with HRV changes that (i) are indicative of a larger cardiac vagal modulation, (ii) are independent from the part of the body needing treatment, (iii) occur even in the absence of musculoskeletal alterations. Yet, many questions remain unanswered, the duration of these effects and the specificity of HRV responses to different OMT techniques being perhaps the most critical. Therefore, this paper discusses prospects for future applications of HRV for the study of the influence of OMT on ANS function. Moreover, based on existing studies and preliminary data on the effects of OMT on HRV in specific pathological (hypertension) and physiological (stress exposure and recovery from sport competition) conditions that are commonly associated with increased sympathetic and/or decreased vagal activity, we propose that HRV analysis could be exploited to evaluate the effectiveness of OMT as a preventive or complementary strategy in clinical and non-clinical conditions characterized by ANS imbalance.
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http://dx.doi.org/10.3389/fnins.2020.579365DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7575744PMC
October 2020

Cortical thickness and resting-state cardiac function across the lifespan: A cross-sectional pooled mega-analysis.

Psychophysiology 2020 Oct 10. Epub 2020 Oct 10.

Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Understanding the association between autonomic nervous system [ANS] function and brain morphology across the lifespan provides important insights into neurovisceral mechanisms underlying health and disease. Resting-state ANS activity, indexed by measures of heart rate [HR] and its variability [HRV] has been associated with brain morphology, particularly cortical thickness [CT]. While findings have been mixed regarding the anatomical distribution and direction of the associations, these inconsistencies may be due to sex and age differences in HR/HRV and CT. Previous studies have been limited by small sample sizes, which impede the assessment of sex differences and aging effects on the association between ANS function and CT. To overcome these limitations, 20 groups worldwide contributed data collected under similar protocols of CT assessment and HR/HRV recording to be pooled in a mega-analysis (N = 1,218 (50.5% female), mean age 36.7 years (range: 12-87)). Findings suggest a decline in HRV as well as CT with increasing age. CT, particularly in the orbitofrontal cortex, explained additional variance in HRV, beyond the effects of aging. This pattern of results may suggest that the decline in HRV with increasing age is related to a decline in orbitofrontal CT. These effects were independent of sex and specific to HRV; with no significant association between CT and HR. Greater CT across the adult lifespan may be vital for the maintenance of healthy cardiac regulation via the ANS-or greater cardiac vagal activity as indirectly reflected in HRV may slow brain atrophy. Findings reveal an important association between CT and cardiac parasympathetic activity with implications for healthy aging and longevity that should be studied further in longitudinal research.
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http://dx.doi.org/10.1111/psyp.13688DOI Listing
October 2020

Bifidobacterium adolescentis as a key member of the human gut microbiota in the production of GABA.

Sci Rep 2020 08 24;10(1):14112. Epub 2020 Aug 24.

Laboratory of Probiogenomics, Department of Chemistry, Life Sciences, and Environmental Sustainability, University of Parma, Parco Area delle Scienze 11a, 43124, Parma, Italy.

Gamma aminobutyric acid (GABA) is the principal inhibitory neurotransmitter playing a key role in anxiety and depression disorders in mammals. Recent studies revealed that members of the gut microbiota are able to produce GABA modulating the gut-brain axis response. Among members of the human gut microbiota, bifidobacteria are well known to establish many metabolic and physiologic interactions with the host. In this study, we performed genome analyses of more than 1,000 bifidobacterial strains publicly available revealing that Bifidobacterium adolescentis taxon might represent a model GABA producer in human gastrointestinal tract. Moreover, the in silico screening of human/animal metagenomic datasets showed an intriguing association/correlation between B. adolescentis load and mental disorders such as depression and anxiety. Interestingly, in vitro screening of 82 B. adolescentis strains allowed identifying two high GABA producers, i.e. B. adolescentis PRL2019 and B. adolescentis HD17T2H, which were employed in an in vivo trial in rats. Feeding Groningen rats with a supplementation of B. adolescentis strains, confirmed the ability of these microorganisms to stimulate the in vivo production of GABA highlighting their potential implication in gut-brain axis interactions.
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http://dx.doi.org/10.1038/s41598-020-70986-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7445748PMC
August 2020

The compassionate vagus: A meta-analysis on the connection between compassion and heart rate variability.

Neurosci Biobehav Rev 2020 09 15;116:21-30. Epub 2020 Jun 15.

Department of Psychology, Sapienza University of Rome, Rome, Italy; Neuroimaging Laboratory, IRCCS Santa Lucia Foundation, Rome, Italy. Electronic address:

In recent years, increasing interest has been devoted to the physiological basis of self and other-oriented compassion. Heart rate variability (HRV) represents a promising candidate for such a role, given its association with soothing emotions and context appropriate prefrontal inhibitory control over threat-defensive responses. The aim of this study was to meta-analyze available studies on the association between compassion and HRV. Random-effect models were used. The analysis performed on sixteen studies that met inclusion criteria, yielded a significant association with a medium effect size (g = .54 95% CI [.24, .84], p < .0001). Results were not influenced by publication bias. After an extreme outlier's exclusion, the size of the association was still larger in studies that used time or frequency-domain indices of vagally-mediated HRV compared to those that used peak to trough estimates of respiratory sinus arrhythmia. Results are limited by the small number of studies included in the meta-analysis (n = 16) and are discussed in terms of indications for future research, given that existing data are highly heterogeneous and of poor methodological rigor.
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http://dx.doi.org/10.1016/j.neubiorev.2020.06.016DOI Listing
September 2020

Antidepressant-like effects of pharmacological inhibition of FAAH activity in socially isolated female rats.

Eur Neuropsychopharmacol 2020 03 13;32:77-87. Epub 2020 Jan 13.

Stress Physiology Lab, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area delle Scienze 11/A, 43124 Parma, Italy. Electronic address:

Pharmacological inhibition of the enzyme fatty acid amide hydrolase (FAAH), which terminates signaling of the endocannabinoid N-arachidonoylethanolamine (or anandamide, AEA), exerts favourable effects in rodent models of stress-related depression. Yet although depression seems to be more common among women than men and in spite of some evidence of sex differences in treatment efficacy, preclinical development of FAAH inhibitors for the pharmacotherapy of stress-related depression has been predominantly conducted in male animals. Here, adult female rats were exposed to six weeks of social isolation and, starting from the second week, treated with the FAAH inhibitor URB694 (0.3 mg/kg/day, i.p.) or vehicle. Compared to pair-housed females, socially isolated female rats treated with vehicle developed behavioral (mild anhedonia, passive stress coping) and physiological (reduced body weight gain, elevated plasma corticosterone levels) alterations. Moreover, prolonged social isolation provoked a reduction in brain-derived neurotrophic factor (BDNF) and AEA levels within the hippocampus. Together, these changes are indicative of an increased risk of developing a depressive-like state. Conversely, pharmacological inhibition of FAAH activity with URB694 restored both AEA and BDNF levels within the hippocampus of socially isolated rats and prevented the development of behavioral and physiological alterations. These results suggest a potential interplay between AEA-mediated signaling and hippocampal BDNF in the pathogenesis of depression-relevant behaviors and physiological alterations and antidepressant action of FAAH inhibition in socially isolated female rats.
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http://dx.doi.org/10.1016/j.euroneuro.2019.12.119DOI Listing
March 2020

The contagion of social defeat stress: Insights from rodent studies.

Neurosci Biobehav Rev 2020 04 10;111:12-18. Epub 2020 Jan 10.

Stress Physiology Lab, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy.

Stressful experiences can be transmitted among individuals through social interactions. Like humans, rodents are social creatures whose behavior and physiology can be influenced by the emotional state of fellow rodents. This paper will review rodent studies which have explored two conditions of potential social stress contagion using the social defeat paradigm. In the vicarious social defeat model, mice and rats that witness a conspecific being socially defeated exhibit physiological stress responses and develop a host of depressive- and anxiety-like behavioral deficits. Likewise, social interaction with a stressed partner in the aftermath of social defeat stress results in physiological stress responses and social avoidance behavior. After summarizing the existing literature on this newly emerging area of social defeat stress contagion in rodents, we will discuss the potential utility of these rodent models for investigating the neurobiological processes and sensory channels of information that allow for the spread of psychophysiological effects of stress across individuals.
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http://dx.doi.org/10.1016/j.neubiorev.2020.01.011DOI Listing
April 2020

Concomitant Evaluation of Heart Period and QT Interval Variability Spectral Markers to Typify Cardiac Control in Humans and Rats.

Front Physiol 2019 29;10:1478. Epub 2019 Nov 29.

Department of Cardiothoracic, Vascular Anesthesia and Intensive Care, IRCCS Policlinico San Donato, Milan, Italy.

The variability of heart period, measured as the time distance between two consecutive QRS complexes from the electrocardiogram (RR), was exploited to infer cardiac vagal control, while the variability of the duration of the electrical activity of the heart, measured as the time interval from Q-wave onset to T-wave end (QT), was proposed as an indirect index of cardiac sympathetic modulation. This study tests the utility of the concomitant evaluation of RR variability (RRV) and QT variability (QTV) markers in typifying cardiac autonomic control of humans under different experimental conditions and of rat groups featuring documented differences in resting sympatho-vagal balance. We considered: (i) 23 healthy young subjects in resting supine position (REST) undergoing head-up tilt at 45° (T45) and 90° (T90) followed by recovery to the supine position; (ii) 9 Wistar (WI) and 14 wild-type Groningen (WT) rats in unstressed conditions, where the WT animals were classified as non-aggressive (non-AGG, = 9) and aggressive (AGG, = 5) according to the resident intruder test. In humans, spectral analysis of RRV and QTV was performed over a single stationary sequence of 250 consecutive values. In rats, spectral analysis was iterated over 10-min recordings with a frame length of 250 beats with 80% overlap and the median of the distribution of the spectral markers was extracted. Over RRV and QTV we computed the power in the low frequency (LF, from 0.04 to 0.15 Hz in humans and from 0.2 to 0.75 Hz in rats) band (LF and LF) and the power in the high frequency (HF, from 0.15 to 0.5 Hz in humans and from 0.75 to 2.5 Hz in rats) band (HF and HF). In humans the HF power was lower during T90 and higher during recovery compared to REST, while the LF power was higher during T90. In rats the HF power was lower in WT rats compared to WI rats and the LF power was higher in AGG than in non-AGG animals. We concluded that RRV and QTV provide complementary information in describing the functioning of vagal and sympathetic limbs of the autonomic nervous system in humans and rats.
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http://dx.doi.org/10.3389/fphys.2019.01478DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6897045PMC
November 2019

Bifidobacterial Transfer from Mother to Child as Examined by an Animal Model.

Microorganisms 2019 Aug 27;7(9). Epub 2019 Aug 27.

Laboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, 43124 Parma, Italy.

Bifidobacteria commonly constitute the most abundant group of microorganisms in the healthy infant gut. Their intestinal establishment is believed to be maternally driven, and their acquisition has even been postulated to occur during pregnancy. In the current study, we evaluated bifidobacterial mother-to infant transmission events in a rat model by means of quantitative PCR (qPCR), as well as by Internally Transcribed Spacer (ITS) bifidobacterial profiling. The occurrence of strains supplied by mothers during pregnancy to their corresponding newborns was observed and identified by analysis immediately following C-section delivery. These findings provide intriguing support for the existence of an unknown route to facilitate bifidobacterial transfer during the very early stages of life.
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http://dx.doi.org/10.3390/microorganisms7090293DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6780879PMC
August 2019

Effects of prefrontal transcranial direct current stimulation on autonomic and neuroendocrine responses to psychosocial stress in healthy humans.

Stress 2020 01 8;23(1):26-36. Epub 2019 Jun 8.

Department of Psychology, Sapienza University of Rome, Rome, Italy.

Prolonged or repeated activation of the stress response can have negative psychological and physical consequences. The prefrontal cortex (PFC) is thought to exert an inhibitory influence on the activity of autonomic and neuroendocrine stress response systems. In this study, we further investigated this hypothesis by increasing PFC excitability using transcranial direct current stimulation (tDCS). Healthy male participants were randomized to receive either anodal (excitatory) tDCS ( = 15) or sham stimulation ( = 15) over the left dorsolateral prefrontal cortex (DLPFC) immediately before and during the exposure to a psychosocial stress test. Autonomic (heart rate (HR) and its variability) and neuroendocrine (salivary cortisol) parameters were assessed. One single session of excitatory tDCS over the left DLPFC (i) reduced HR and favored a larger vagal prevalence prior to stress exposure, (ii) moderated stress-induced HR acceleration and sympathetic activation/vagal withdrawal, but (iii) had no effect on stress-induced cortisol release. However, anodal tDCS over the left DLPFC prevented stress-induced changes in the cortisol awakening response. Finally, participants receiving excitatory tDCS reported a reduction in their levels of state anxiety upon completion of the psychosocial stress test. In conclusion, this study provides first insights into the efficacy of one single session of excitatory tDCS over the left DLPFC in attenuating autonomic and neuroendocrine effects of psychosocial stress exposure. These findings might be indicative of the important role of the left DLPFC, which is a cortical target for noninvasive brain stimulation treatment of depression, for successful coping with stressful stimuli.
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http://dx.doi.org/10.1080/10253890.2019.1625884DOI Listing
January 2020

Exploring the effects of COLOSTRONONI on the mammalian gut microbiota composition.

PLoS One 2019 31;14(5):e0217609. Epub 2019 May 31.

Laboratory of Probiogenomics, Department of Chemistry, Life Sciences, and Environmental Sustainability, University of Parma, Parma, Italy.

COLOSTRONONI is a dietary supplement consisting of bovine colostrum and Morinda citrifolia fruit (Noni). In this study, we tested the capability of COLOSTRONONI to influence gut microbiota composition using an in vivo evaluation in rats. Furthermore, we analyzed the effect of COLOSTRONONI on the systemic inflammatory responses as well as on the gut permeability of the animals. Altogether, our analyses supported the concept of COLOSTRONONI as a natural food supplement that doesn't affect (neither negatively nor positively) gut microbiota homeostasis in healthy conditions. Moreover, COLOSTRONONI highlighted a lower effect in the expression of genes coding for IL-10, Il-12 and TNF-α response allowing us to hypothesize an immunomodulatory activity of this dietary supplement.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0217609PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6544264PMC
January 2020

Resting Heart Rate Variability Predicts Vulnerability to Pharmacologically-Induced Ventricular Arrhythmias in Male Rats.

J Clin Med 2019 May 10;8(5). Epub 2019 May 10.

Stress Physiology Lab, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, 43121 Parma, Italy.

The electrical stability of the myocardium is dependent on the dynamic balance between sympathetic and parasympathetic influences on the heart, which is reflected by heart rate variability (HRV). Reduced HRV is a proposed predictor of sudden death caused by ventricular tachyarrhythmias in cardiac patients. However, the link between individual differences in HRV and ventricular tachyarrhythmic risk in populations without known pre-existing cardiac conditions is less well explored. In this study we investigated the extent to which individual differences in resting state HRV predict susceptibility to spontaneous and pharmacologically-induced ventricular arrhythmias in healthy rats. Radiotelemetric transmitters were implanted in 42 adult male Wild-type Groningen rats. ECG signals were recorded during 24-h resting conditions and under β-adrenoceptor pharmacological stimulation with isoproterenol and analyzed by means of time- and frequency-domain indexes of HRV. No significant association was found between individual differences in resting measures of HRV and spontaneous incidence of ventricular arrhythmias. However, lower resting values of HRV predicted a higher number of ventricular ectopic beats following β-adrenergic pharmacological stimulation with isoproterenol (0.02 mg/kg). Moreover, after isoproterenol administration, one rat with low resting HRV developed sustained ventricular tachycardia that led to death. The present results might be indicative of the potential utility of HRV measures of resting cardiac autonomic function for the prediction of ventricular arrhythmias, particularly during conditions of strong sympathetic activation, in populations without known cardiac disease.
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http://dx.doi.org/10.3390/jcm8050655DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6572182PMC
May 2019

Psychological characteristics and physiological reactivity to acute stress in mothers of children with autism spectrum disorder.

Stress Health 2019 Oct 20;35(4):421-431. Epub 2019 Jun 20.

Stress Physiology Lab, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy.

Stress related to parenting a child with autism spectrum disorder can differently affect caregiver's physiological reactivity to acute stress. Here, parental stress levels, psychological characteristics, and coping strategies were assessed alongside measures of heart rate, heart rate variability, and cortisol during a psychosocial stress test in mothers of children with ASD (M-ASD, n = 15) and mothers of typically developing children (n = 15). M-ASD reported significantly higher levels of parental stress, anxiety, negative affectivity, social inhibition, and a larger preference for avoidance strategies. M-ASD showed larger heart rate and cortisol responses to the psychosocial stress test. A positive relationship was found between parental stress levels and the magnitude of the cortisol stress response in both groups. The present findings indicate exaggerated physiological reactivity to acute psychosocial stress in M-ASD and prompt further research to explore the role of individual differences in mediating the effects of parental stress on physiological stress responses.
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http://dx.doi.org/10.1002/smi.2870DOI Listing
October 2019

Ability of bifidobacteria to metabolize chitin-glucan and its impact on the gut microbiota.

Sci Rep 2019 04 8;9(1):5755. Epub 2019 Apr 8.

Department of Veterinary Medical Science, University of Parma, Parma, Italy.

Chitin-glucan (CG) represents a natural carbohydrate source for certain microbial inhabitants of the human gut and may act as a prebiotic for a number of bacterial taxa. However, the bifidogenic activity of this substrate is still unknown. In the current study, we evaluated the ability of chitin-glucan to influence growth of 100 bifidobacterial strains belonging to those species commonly identified within the bifidobacterial communities residing in the infant and adult human gut. Such analyses were coupled with transcriptome experiments directed to explore the transcriptional effects of CG on Bifidobacterium breve 2L, which was shown to elicit the highest growth performance on this natural polysaccharide. In addition, an in vivo trial involving a rat model revealed how the colonization efficiency of this bifidobacterial strain was enhanced when the animals were fed with a diet containing CG. Altogether our analyses indicate that CG is a valuable novel prebiotic compound that may be added to the human diet in order to re-establish/reinforce bifidobacteria colonization in the mammalian gut.
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http://dx.doi.org/10.1038/s41598-019-42257-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6453949PMC
April 2019

Febrile and sleep responses to an immune challenge are affected by trait aggressiveness in rats.

Brain Behav Immun 2019 08 3;80:300-307. Epub 2019 Apr 3.

Department of Health Sciences, University of Milan Medical School, Milan, Italy. Electronic address:

Sleep is altered in response to an immune challenge: non-rapid eye movement (NREM) sleep is increased and fragmented, REM sleep is inhibited. Sleep and immune response are affected by stress: several stressors inhibit sleep and increase waking time; stress-induced cortisol secretion affects the immune response, with immunosuppressive effects. Different levels of trait aggressiveness are associated with specific patterns of neuroendocrine and autonomic stress responsiveness. Aim of this study was to test the hypothesis that trait aggressiveness, by affecting response to stressors, modifies sleep alterations induced by the activation of the immune response. To this aim, rats were selected on the basis of their latency time to attack a male intruder in the resident-intruder test. Animals were instrumented for chronic recordings of sleep-wake activity and injected, intraperitoneally, with an immune challenge (250 μg/kg lipopolysaccharide - LPS, a component of gram-negative bacterial cell wall). Here we report that high aggressive (HA) rats responded to an immune challenge with a 24-h long increase in cortical brain temperature. During the first 12 post-injection hours, HA rats also responded with a prolonged increase in NREM sleep amount, and a 5-h long and continuous inhibition of REM sleep. In HA rats, the LPS-induced increase in the amount of time spent in NREM sleep was due to an increase in the number of episodes of this sleep phase, without any change in the bout duration. The LPS-induced REM sleep inhibition observed in HA rats was due to a decrease in both the number and duration of REM sleep bouts. In HA rats, during REM sleep, LPS administration significantly reduced the power of the EEG theta band. In non-aggressive (NA) rats, in response to LPS administration, cortical brain temperature was increased only for two hours, NREM sleep was unaffected, and REM sleep inhibition was scattered along the first 8 post-injection hours. The LPS-induced changes in the number of NREM sleep bouts of NA rats were limited to few and scattered hours, with a change in bout duration only in a single hour. A combination of decreases, in few hours, in both REM sleep bouts and their duration contributed to the REM sleep inhibition observed in NA rats. In NA rats, the power of EEG theta band was not modified, during REM sleep, by LPS administration. Gross motor activity was inhibited in both HA and NA rats. Results of this study show that trait aggressiveness affects febrile and sleep responses to an immune challenge.
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http://dx.doi.org/10.1016/j.bbi.2019.04.007DOI Listing
August 2019

Heart rate variability and inflammation: A meta-analysis of human studies.

Brain Behav Immun 2019 08 11;80:219-226. Epub 2019 Mar 11.

Department of Psychology, The Ohio State University, Columbus, OH, United States.

The inflammatory reflex is known as the body's primary defense against infection and has been implicated in a number of diseases. The magnitude of the inflammatory response is important, as an extreme or insufficient response can be differentially harmful to the individual. Converging evidence suggests that the autonomic nervous system (ANS) regulates the inflammatory reflex. Heart rate variability (HRV) can be separated into components that primarily reflect parasympathetic (PNS) or vagal activity (i.e., indices of vagally mediated HRV) and a combination of both sympathetic (SNS) and PNS influences. Given the physiological relation between the vagus and inflammatory processes, one would expect to find higher HRV, especially indices of vagally-mediated HRV, to be associated with decreased levels of inflammation via the cholinergic anti-inflammatory pathway. However, existing findings here are mixed, such that studies have also shown a positive association between indices of HRV and markers of inflammation. Therefore, the present meta-analysis aimed to synthesize existing studies, estimating the general direction and strength of the relationship between different indices of HRV and inflammatory markers. A systematic search of the literature yielded 2283 studies that were screened for inclusion eligibility (159 studies eligible for inclusion); in sum, 51 studies reported/provided adequate information for inclusion in meta-analyses. Results generally showed negative associations between indices of HRV and markers of inflammation. In this regard, the standard deviation of R-R intervals (SDNN) and power in the high frequency band of HRV (HF-HRV) showed the strongest and most robust associations with inflammatory markers compared to other time- and frequency-domain measures of HRV. Overall, we propose that indices of HRV can be used to index activity of the neurophysiological pathway responsible for adaptively regulating inflammatory processes in humans.
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http://dx.doi.org/10.1016/j.bbi.2019.03.009DOI Listing
August 2019

Cortical morphometric predictors of autonomic dysfunction in generalized anxiety disorder.

Auton Neurosci 2019 03 4;217:41-48. Epub 2019 Jan 4.

Department of Psychology, Sapienza University of Rome, Italy; Neuroimaging Laboratory, Santa Lucia Foundation, Rome, Italy. Electronic address:

Generalized anxiety disorder (GAD) is associated with both autonomic dysfunction, notably decreased vagally-mediated heart rate variability (vmHRV), and neurostructural abnormalities. Regional differences in brain morphometry correlate with vmHRV in healthy individuals. Here, we tested the hypothesis that specific focal abnormalities in cortical structure in GAD underpin decreased vmHRV. Adult female patients with GAD (n = 17) and matched controls (n = 18) underwent structural magnetic resonance imaging after characterization of symptoms and quantification of resting vmHRV derived from continuous pulse oximetry. Cortical reconstruction was performed using the FreeSurfer image analysis suite. A priori analysis was conducted only within brain regions involved in vagal control of heart rate. Compared to controls, patients with GAD showed cortical thinning of the (i) left rostral anterior cingulate cortex, (ii) left medial orbitofrontal cortex, and (iii) right isthmus cingulate gyrus. Significant negative relationships were identified between the severity of anxiety symptoms and cortical thickness of the left medial orbitofrontal cortex and right isthmus cingulate gyrus. Compared to controls, patients with GAD showed decreased vmHRV at rest. In controls only, cortical thickness of the left caudal anterior cingulate cortex correlated positively with resting vmHRV. These results extend evidence in GAD for structural abnormalities within cortical areas implicated in emotion regulation and cognition. In addition, these findings may implicate abnormal integrity of anterior cingulate cortex in the psychophysiological expression of GAD and suggest that interventional targeting of this region may normalize autonomic function in GAD.
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http://dx.doi.org/10.1016/j.autneu.2019.01.001DOI Listing
March 2019

Hemodynamic profile and compensation deficit in African and European Americans during physical and mental stress.

Biol Psychol 2019 02 30;141:17-24. Epub 2018 Dec 30.

Department of Psychiatry and Behavioral Sciences, Duke University Medical Center, Durham, NC, USA; Center for Biobehavioral Health Disparities Research, Duke University, Durham, NC, USA; Center for the Study of Aging and Human Development, Duke University, Durham, NC, USA.

Increased vascular reactivity to stress has been suggested to contribute to the greater risk for developing hypertension in African Americans. Here, we examined the way (hemodynamic profile) and the extent to which (compensation deficit) cardiac output and total peripheral resistance compensate for each other in determining blood pressure responses to a physical (orthostasis) and a mental (anger recall) stress task, in normotensive African American (AA, n = 30) and European American (EA, n = 48) college students. Blood pressure stress reactivity did not differ as a function of race. However, AAs showed a prominent vascular hemodynamic profile and a significant compensation deficit in response to both tasks, while EAs showed no hemodynamic response to orthostasis and a mixed profile in response to anger recall. The present findings demonstrate a more prominent vascular hemodynamic reactivity to stress in AAs, which could contribute to the pathogenesis of hypertension in this ethnic group.
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http://dx.doi.org/10.1016/j.biopsycho.2018.12.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6830506PMC
February 2019

Low vagal tone in two rat models of psychopathology involving high or low corticosterone stress responses.

Psychoneuroendocrinology 2019 03 3;101:101-110. Epub 2018 Nov 3.

Laboratory of Behavioral Genetics, Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland. Electronic address:

The two stress-responsive physiological systems, autonomic nervous system (ANS) and hypothalamus-pituitary-adrenal (HPA) axis exert complementary and interrelated actions in the organism. Individuals that suffer stress-related psychopathologies frequently present simultaneous alterations -i.e., either low or high- responsiveness- in both systems. However, there is scarce evidence establishing whether a priori alterations in these systems -i.e., independent of previous stress exposure- may predispose to the development of psychopathologies possibly due to the lack of animal models simultaneously involving aberrant HPA and SNS responses. In this study, we describe two animal models selectively bred according to their differential (either high, 'High', or low, 'Low') glucocorticoid responsiveness to stress, in comparison to a third line of rats that displays intermediate ('Inter') glucocorticoid responses. The two extreme lines may be considered distinct models of psychopathology; the High line representing a model of constitutive mood alterations while the Low line a model of vulnerability to develop stress-induced psychopathologies. We recorded the electrocardiogram in rats from the three lines and quantified heart rate variability and vagal tone indexes during rest and stress challenges. Rats from both High and Low lines displayed higher heart rate and lower basal vagal tone than the Inter group, both at resting and following stress exposure. Specific pharmacological manipulations probing the relative contribution of sympathetic and parasympathetic components on HR modulation confirmed a relative lower vagal tone in High and Low lines and discarded differences in the sympathetic regulation of heart rate between the lines. Therefore, the two genetically-selected High and Low glucocorticoid rat lines emerge as two valuable preclinical models of psychopathology involving two key risk factors for psychiatric and cardiovascular disorders, namely dysregulations in the HPA axis and cardiac vagal functioning.
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http://dx.doi.org/10.1016/j.psyneuen.2018.11.003DOI Listing
March 2019

Heart rate variability in neonatal patients with seizures.

Clin Neurophysiol 2018 12 25;129(12):2534-2540. Epub 2018 Oct 25.

Department of Chemistry, Life Sciences and Environmental Sustainability, Stress Physiology Lab, University of Parma, Italy. Electronic address:

Objective: Seizures are frequently observed in neurological conditions affecting newborns. Since autonomic alterations are commonly associated with neonatal seizures (NS), we investigated the utility of heart rate variability (HRV) indexes of cardiac autonomic regulation for NS detection.

Methods: HRV analysis was conducted on ECG tracings recorded during video-EEG monitoring in newborns with NS and matched-controls. The effects of gestational age on HRV were also evaluated.

Results: Newborns with NS showed lower resting state HRV compared to controls. Moreover, seizure episodes were characterized by a short-lasting increase in vagal indexes of HRV. Pre-term newborns with NS had a lower HRV than full-term at rest. In pre-term newborns, no changes in HRV were observed before and during NS. On the contrary, full-term newborns showed significantly higher HRV before and during NS compared to the respective baseline values.

Conclusion: Our data point to resting autonomic impairment in newborns with NS. In addition, an increment in HRV has been observed during NS only in full term newborns.

Significance: Although these findings do not allow validation of HRV measures for NS prediction and detection, they suggest that a putative protective vagal mechanism might be adopted when an advanced maturation of autonomic nervous system is achieved.
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http://dx.doi.org/10.1016/j.clinph.2018.10.001DOI Listing
December 2018

The Utility of Rodent Models of Stress for Disentangling Individual Vulnerability to Depression and Cardiovascular Comorbidity.

Curr Cardiol Rep 2018 09 26;20(11):111. Epub 2018 Sep 26.

Department of Chemistry, Stress Physiology Lab, Life Sciences and Environmental Sustainability, University of Parma, Parco Area delle Scienze 11/A, 43124, Parma, Italy.

Purpose Of Review: This review offers a perspective of the utility of rodent models of stress for identifying sources of individual vulnerability to depression and cardiovascular disease comorbidity.

Recent Findings: Differential stress susceptibility is found in rodents exposed to repeated social defeat as a function of their coping style. Specifically, passive coping rodents show an increase in inflammatory processes within the brain that favour the development of depressive-like symptoms and cardiovascular abnormalities. Similarly, only a sub-group of rats develops depressive-like symptoms following chronic mild stress exposure. Cardiovascular changes differ depending on individual stress susceptibility and may be related to an imbalance in the autonomic regulation of cardiac function in stress vulnerable subjects. Rodent models of stress that take into account individual phenotypic variations are useful for a better understanding of the role of neuroinflammatory and autonomic processes in the development of comorbid depression and cardiovascular disease under stressful conditions.
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http://dx.doi.org/10.1007/s11886-018-1064-xDOI Listing
September 2018

Autonomic and Brain Morphological Predictors of Stress Resilience.

Front Neurosci 2018 6;12:228. Epub 2018 Apr 6.

Neuroimaging Laboratory, Santa Lucia Foundation, Rome, Italy.

Stressful life events are an important cause of psychopathology. Humans exposed to aversive or stressful experiences show considerable inter-individual heterogeneity in their responses. However, the majority does not develop stress-related psychiatric disorders. The dynamic processes encompassing positive and functional adaptation in the face of significant adversity have been broadly defined as . Traditionally, the assessment of resilience has been confined to self-report measures, both within the general community and putative high-risk populations. Although this approach has value, it is highly susceptible to subjective bias and may not capture the dynamic nature of resilience, as underlying construct. Recognizing the obvious benefits of more objective measures of resilience, research in the field has just started investigating the predictive value of several potential biological markers. This review provides an overview of theoretical views and empirical evidence suggesting that individual differences in heart rate variability (HRV), a surrogate index of resting cardiac vagal outflow, may underlie different levels of resilience toward the development of stress-related psychiatric disorders. Following this line of thought, recent studies describing associations between regional brain morphometric characteristics and resting state vagally-mediated HRV are summarized. Existing studies suggest that the structural morphology of the anterior cingulated cortex (ACC), particularly its cortical thickness, is implicated in the expression of individual differences in HRV. These findings are discussed in light of emerging structural neuroimaging research, linking morphological characteristics of the ACC to psychological traits ascribed to a high-resilient profile and abnormal structural integrity of the ACC to the psychophysiological expression of stress-related mental health consequences. We conclude that a multidisciplinary approach integrating brain structural imaging with HRV monitoring could offer novel perspectives about brain-body pathways in resilience and adaptation to psychological stress.
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http://dx.doi.org/10.3389/fnins.2018.00228DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5897537PMC
April 2018

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

Int J Psychophysiol 2018 09 5;131:131-138. Epub 2017 Nov 5.

Neuroimaging Laboratory, Santa Lucia Foundation, Rome, Italy; Department of Psychology, Sapienza University of Rome, Italy. Electronic address:

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 and Time 2 (~13 and 34months after Time 0, respectively). Ruminative thinking was found to be (i) a stable trait characteristic, (ii) more prevalent in women than men, and (iii) positively correlated with depressive symptoms. Moreover, resting HRV was negatively correlated with both rumination and depressive symptoms. Finally, HRV at Time 1 mediated the relationship between rumination at Time 0 and depressive symptoms at Time 2. We conclude that autonomic dysfunction, specifically low vagal tone, may be prospectively implicated in the generation of depressive symptoms in a non-clinical setting.
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http://dx.doi.org/10.1016/j.ijpsycho.2017.11.002DOI Listing
September 2018

How to Feed the Mammalian Gut Microbiota: Bacterial and Metabolic Modulation by Dietary Fibers.

Front Microbiol 2017 12;8:1749. Epub 2017 Sep 12.

Laboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of ParmaParma, Italy.

The composition of the gut microbiota of mammals is greatly influenced by diet. Therefore, evaluation of different food ingredients that may promote changes in the gut microbiota composition is an attractive approach to treat microbiota disturbances. In this study, three dietary fibers, such as inulin (I, 10%), resistant starch (RS, 10%), and citrus pectin (3%), were employed as supplements to normal chow diet of adult male rats for 2 weeks. Fecal microbiota composition and corresponding metabolite profiles were assessed before and after prebiotics supplementation. A general increase in the phylum was detected with a concurrent reduction in , in particular for I and RS experiments, while additional changes in the microbiota composition were evident at lower taxonomic levels for all the three substrates. Such modifications in the microbiota composition were correlated with changes in metabolic profiles of animals, in particular changes in acetate and succinate levels. This study represents a first attempt to modulate selectively the abundance and/or metabolic activity of various members of the gut microbiota by means of dietary fiber.
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http://dx.doi.org/10.3389/fmicb.2017.01749DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5600934PMC
September 2017

Single Osteopathic Manipulative Therapy Session Dampens Acute Autonomic and Neuroendocrine Responses to Mental Stress in Healthy Male Participants.

J Am Osteopath Assoc 2017 Sep;117(9):559-567

Context: The efficacy of osteopathic manipulative therapy (OMTh; manipulative care provided by foreign-trained osteopaths) is supported by observational data and patient feedback, but there is still a need for objective, quantitative biomarkers that allow measurement of the underlying mechanisms. No study exploring the protective potential of OMTh for mental stress has been published, to the authors' knowledge.

Objectives: To explore the modulating effect of OMTh on autonomic neural regulation of the heart and verifiy its ability to influence the activity of the hypothalmic-pituitary-adrenocortical axis.

Methods: Healthy young adult men who had never received OMTh were exposed to either a brief protocol using craniosacral techniques or sham therapy (control) involving the same anatomical areas. A laboratory stress episode consisting of a 5-minute arithmetic task participants were required to perform in front of a committee preceded the therapy sessions. Continuous electrocardiograph recordings were done before, during, and after the stress episode. Heart rate and frequency-domain parameters of heart rate variability (specifically, high-frequency component power in normalized units and the ratio of low-frequency to high-frequency power) were measured to quantify the activity of the parasympathetic nervous system and the state of sympathovagal balance at the level of the heart, respectively. Saliva samples were also collected at points throughout the study to determine cortisol levels.

Results: Osteopathic manipulative therapy reduced the overall chronotropic effect of the stressor (t=-2.9, P<.05) and counteracted the vagal withdrawal and the shift of autonomic balance toward sympathetic prevalence (t=-2.8, P<.05) that were observed in control participants. Moreover, OMTh participants had a much lower overall cortisol level during the mental stressor compared with control participants (t=-2.3, P<.05). Participants in the OMTh group did not show the statistically significant reduction in the amplitude of the cortisol awakening response observed in their control counterparts after the stress episode (control: t=2.7, P<.05; OMT: P=.83).

Conclusion: The application of a single OMTh session to healthy participants induced a faster recovery of heart rate and sympathovagal balance after an acute mental stressor by substantially dampening parasympathetic withdrawal and sympathetic prevalence. The OMTh session also prevented the typical increase in cortisol levels observed immediately after a brief mental challenge.
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http://dx.doi.org/10.7556/jaoa.2017.110DOI Listing
September 2017

Social stress contagion in rats: Behavioural, autonomic and neuroendocrine correlates.

Psychoneuroendocrinology 2017 Aug 20;82:155-163. Epub 2017 May 20.

Department of Chemistry, Life Sciences and Environmental Sustainability, Stress Physiology Lab, University of Parma, Italy. Electronic address:

The negative emotional consequences associated with life stress exposure in an individual can affect the emotional state of social partners. In this study, we describe an experimental rat model of social stress contagion and its effects on social behaviour and cardiac autonomic and neuroendocrine functions. Adult male Wistar rats were pair-housed and one animal (designated as "demonstrator" (DEM)) was submitted to either social defeat stress (STR) by an aggressive male Wild-type rat in a separate room or just exposed to an unfamiliar empty cage (control condition, CTR), once a day for 4 consecutive days. We evaluated the influence of cohabitation with a STR DEM on behavioural, cardiac autonomic and neuroendocrine outcomes in the cagemate (defined "observer" (OBS)). After repeated social stress, STR DEM rats showed clear signs of social avoidance when tested in a new social context compared to CTR DEM rats. Interestingly, also their cagemate STR OBSs showed higher levels of social avoidance compared to CTR OBSs. Moreover, STR OBS rats exhibited a higher heart rate and a larger shift of cardiac autonomic balance toward sympathetic prevalence (as indexed by heart rate variability analysis) immediately after the first reunification with their STR DEMs, compared to the control condition. This heightened cardiac autonomic responsiveness habituated over time. Finally, STR OBSs showed elevated plasma corticosterone levels at the end of the experimental protocol compared to CTR OBSs. These findings demonstrate that cohabitation with a DEM rat, which has experienced repeated social defeat stress, substantially disrupts social behaviour and induces short-lasting cardiac autonomic activation and hypothalamic-pituitary-adrenal axis hyperactivity in the OBS rat, thus suggesting emotional state-matching between the OBS and the DEM rats. We conclude that this rodent model may be further exploited for investigating the neurobiological bases of negative affective sharing between social partners under chronic social stress conditions.
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http://dx.doi.org/10.1016/j.psyneuen.2017.05.017DOI Listing
August 2017

Rodent models of depression-cardiovascular comorbidity: Bridging the known to the new.

Neurosci Biobehav Rev 2017 05 16;76(Pt A):144-153. Epub 2017 Jan 16.

Stress Physiology Lab., Department of Neuroscience, University of Parma, Italy. Electronic address:

Numerous epidemiological studies have demonstrated a close and bidirectional association between depression and cardiovascular disorders (CVD). This comorbidity places a significant burden on individuals and the healthcare system. Not surprisingly, in the last two decades preclinical research in the field of depression and CVD has rapidly progressed. Multiple studies have demonstrated that aspects of human depression/cardiovascular comorbidity can be modeled in rodents exposed to chronic stress paradigms and that a depressive-like syndrome can be induced in rodent models of CVD. This research has provided insights into neural, autonomic, humoral, immune and circulatory mechanisms linking co-occurring mood and CVD. Recent investigations have started to address gender and individual differences in the vulnerability to both disorders and have begun to explore the efficacy of novel pharmacological interventions for the treatment of these comorbid conditions. This review discusses relatively well-established findings and the latest discoveries from rodent models of depression and CVD, with the aim of providing an up-to-date reference which may guide future studies of the relationship between mood and cardiovascular disturbances.
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http://dx.doi.org/10.1016/j.neubiorev.2016.11.006DOI Listing
May 2017