Publications by authors named "Hugo D Critchley"

182 Publications

Beyond bones: The relevance of variants of connective tissue (hypermobility) to fibromyalgia, ME/CFS and controversies surrounding diagnostic classification: an observational study.

Clin Med (Lond) 2021 Jan;21(1):53-58

Brighton and Sussex University Hospitals NHS Trust, Brighton, UK and Brighton and Sussex Medical School, Falmer, UK.

Background: Fibromyalgia and myalgic encephalomyelitis / chronic fatigue syndrome (ME/CFS) are poorly understood conditions with overlapping symptoms, fuelling debate as to whether they are manifestations of the same spectrum or separate entities. Both are associated with hypermobility, but this remains significantly undiagnosed, despite impact on quality of life.

Objective: We planned to understand the relevance of hypermobility to symptoms in fibromyalgia and ME/CFS.

Method: Sixty-three patient participants presented with a confirmed diagnosis of fibromyalgia and/or ME/CFS; 24 participants were healthy controls. Patients were assessed for symptomatic hypermobility.

Results: Evaluations showed exceptional overlap in patients between fibromyalgia and ME/CFS, plus 81% met Brighton criteria for hypermobility syndrome (odds ratio 7.08) and 18% met 2017 hypermobile Ehlers-Danlos syndrome (hEDS) criteria. Hypermobility scores significantly predicted symptom levels.

Conclusion: Symptomatic hypermobility is particularly relevant to fibromyalgia and ME/CFS, and our findings highlight high rates of mis-/underdiagnosis. These poorly understood conditions have a considerable impact on quality of life and our observations have implications for diagnosis and treatment targets.
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http://dx.doi.org/10.7861/clinmed.2020-0743DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7850199PMC
January 2021

Amplified engagement of prefrontal cortex during control of voluntary action in Tourette syndrome.

Brain Commun 2020 27;2(2):fcaa199. Epub 2020 Nov 27.

Sackler Centre for Consciousness Science, University of Sussex, Sussex, UK.

Tourette syndrome is characterized by 'unvoluntary' tics, which are compulsive, yet often temporarily suppressible. The inferior frontal gyrus is implicated in motor control, including inhibition of pre-potent actions through influences on downstream subcortical and motor regions. Although tic suppression in Tourette syndrome also engages the inferior frontal gyrus, it is unclear whether such prefrontal control of action is also dysfunctional: Tic suppression studies do not permit comparison with control groups, and neuroimaging studies of motor inhibition can be confounded by the concurrent expression or suppression of tics. Here, patients with Tourette syndrome were directly compared to control participants when performing an intentional inhibition task during functional MRI. Tic expression was recorded throughout for removal from statistical models. Participants were instructed to make a button press in response to Go cues, withhold responses to NoGo cues, and decide whether to press or withhold to 'Choose' cues. Overall performance was similar between groups, for both intentional inhibition rates (% Choose-Go) and reactive NoGo inhibition commission errors. A subliminal face prime elicited no additional effects on intentional or reactive inhibition. Across participants, the task activated prefrontal and motor cortices and subcortical nuclei, including pre-supplementary motor area, inferior frontal gyrus, insula, caudate nucleus, thalamus and primary motor cortex. In Tourette syndrome, activity was elevated in the inferior frontal gyrus, insula and basal ganglia, most notably within the right inferior frontal gyrus during voluntary action and inhibition (Choose-Go and Choose-NoGo), and reactive inhibition (NoGo-correct). Anatomically, the locus of this inferior frontal gyrus hyperactivation during control of voluntary action matched that previously reported for tic suppression. In Tourette syndrome, activity within the caudate nucleus was also enhanced during both intentional (Choose-NoGo) and reactive (NoGo-correct) inhibition. Strikingly, despite the absence of overt motor behaviour, primary motor cortex activity increased in patients with Tourette syndrome but decreased in controls during both reactive and intentional inhibition. Additionally, severity of premonitory sensations scaled with functional connectivity of the pre-supplementary motor area to the caudate nucleus, globus pallidus and thalamus when choosing to respond (Choose-Go). Together, these results suggest that patients with Tourette syndrome use equivalent prefrontal mechanisms to suppress tics and withhold non-tic actions, but require greater inferior frontal gyrus engagement than controls to overcome motor drive from hyperactive downstream regions, notably primary motor cortex. Moreover, premonitory sensations may cue midline motor regions to generate tics through interactions with the basal ganglia.
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http://dx.doi.org/10.1093/braincomms/fcaa199DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7772099PMC
November 2020

Diseases, Disorders, and Comorbidities of Interoception.

Trends Neurosci 2021 01;44(1):39-51

Department of Neuroscience, Brighton and Sussex Medical School, Brighton, UK.

Interoception, the sense of the body's internal physiological state, underpins homeostatic reflexes, motivational states, and sensations contributing to emotional experiences. The continuous nature of interoceptive processing, coupled to behavior, is implicated in the neurobiological construction of the sense of self. Aberrant integration and control of interoceptive signals, originating in the brain and/or the periphery, can perturb the whole system. Interoceptive abnormalities are implicated in the pathophysiology of psychiatric disorders and in the symptomatic expression of developmental, neurodegenerative, and neurological disorders. Moreover, interoceptive mechanisms appear central to somatic disorders of brain-body interactions, including functional digestive disorders, chronic pain, and comorbid conditions. The present article provides an overview of disorders of interoception and suggests future directions for better understanding, diagnosis, and management of these disorders.
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http://dx.doi.org/10.1016/j.tins.2020.09.009DOI Listing
January 2021

Corrigendum to "Differential brain responses for perception of pain during empathic response in binge drinkers compared to non-binge drinkers" [Neuroimage Clin., 27 (2020) 1-11/102322].

Neuroimage Clin 2020 4;28:102448. Epub 2020 Dec 4.

Behavioural and Clinical Neuroscience, School of Psychology, University of Sussex, United Kingdom; Clinical Imaging Sciences Centre, Brighton and Sussex Medical School, University of Sussex, United Kingdom. Electronic address:

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http://dx.doi.org/10.1016/j.nicl.2020.102448DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7752702PMC
December 2020

Interoceptive cardiac signals selectively enhance fear memories.

J Exp Psychol Gen 2020 Nov 12. Epub 2020 Nov 12.

Brighton and Sussex Medical School.

Fear is coupled to states of physiological arousal. We tested how learning and memory of threat, specifically conditioned fear, is influenced by interoceptive signals. Forty healthy individuals were exposed to two threat (conditioned stimuli [CS+], paired with electrocutaneous shocks) and two safety (CS-) stimuli, time-locked to either cardiac ventricular systole (when arterial baroreceptors signal cardiovascular arousal to brainstem), or diastole (when these afferent signals are quiescent). Threat learning was indexed objectively using skin conductance responses (SCRs). During acquisition of threat contingencies, cardiac effects dominated: Stimuli (both CS+ and CS-) presented at systole evoked greater SCR responses, relative to stimuli (both CS+ and CS-) presented at diastole. This difference was amplified in more anxious individuals. Learning of conditioned fear was established by the end of the acquisition phase, which was followed by an extinction phase when unpaired CSs were presented at either the same or switched cardiac contingencies. One day later, electrocutaneous shocks triggered the reinstatement of fear responses. Subsequent presentation of stimuli previously encoded at systole evoked higher SCRs. Moreover, only those participants for whom stimuli had the same cardiac-contingency over both acquisition and extinction phases retained conditioned fear memory (i.e., CS+ > CS-). Our findings reveal two important cardiac afferent effects on threat learning and memory: 1) Cardiac signals bias processing toward threat; and 2) cardiac signals are a context for fear memory; altering this context can disrupt the memory. These observations suggest how threat reactivity may be reinforced and maintained by both acute and enduring states of cardiac arousal. (PsycInfo Database Record (c) 2020 APA, all rights reserved).
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http://dx.doi.org/10.1037/xge0000967DOI Listing
November 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

Trait Impulsivity Associated With Altered Resting-State Functional Connectivity Within the Somatomotor Network.

Front Behav Neurosci 2020 24;14:111. Epub 2020 Jun 24.

Behavioural and Clinical Neuroscience, University of Sussex, Brighton, United Kingdom.

Knowledge of brain mechanisms underlying self-regulation can provide valuable insights into how people regulate their thoughts, behaviors, and emotional states, and what happens when such regulation fails. Self-regulation is supported by coordinated interactions of brain systems. Hence, behavioral dysregulation, and its expression as impulsivity, can be usefully characterized using functional connectivity methodologies applied to resting brain networks. The current study tested whether individual differences in trait impulsivity are reflected in the functional architecture within and between resting-state brain networks. Thirty healthy individuals completed a self-report measure of trait impulsivity and underwent resting-state functional magnetic resonance imaging. Using Probabilistic Independent Components Analysis in FSL MELODIC, we identified across participants 10 networks of regions (resting-state networks) with temporally correlated time courses. We then explored how individual expression of these spatial networks covaried with trait impulsivity. Across participants, we observed that greater self-reported impulsivity was associated with decreased connectivity of the right lateral occipital cortex (peak mm 46/-70/16, FWE 1- = 0.981) with the somatomotor network. No supratheshold differences were observed in between-network connectivity. Our findings implicate the somatomotor network, and its interaction with sensory cortices, in the control of (self-reported) impulsivity. The observed "decoupling" may compromise effective integration of early perceptual information (from visual and somatosensory cortices) with behavioral control programs, potentially resulting in negative consequences.
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http://dx.doi.org/10.3389/fnbeh.2020.00111DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7326939PMC
June 2020

Differential brain responses for perception of pain during empathic response in binge drinkers compared to non-binge drinkers.

Neuroimage Clin 2020 25;27:102322. Epub 2020 Jun 25.

Behavioural and Clinical Neuroscience, School of Psychology, University of Sussex, United Kingdom; Clinical Imaging Sciences Centre, Brighton and Sussex Medical School, University of Sussex, United Kingdom. Electronic address:

Individuals who engage in binge drinking behaviors may show evidence of impaired cognitive function and emotional dysregulation. Impaired empathy, characterized by a reduced ability to understand and respond appropriately to feelings of others, is increasingly recognized for its role in Alcohol Use Disorders (AUD). The present study examined a population of young adult social drinkers to compare individuals who show binge drinking behavior to those who do not on measures of empathic processing and associated neural responses. A secondary aim explored similarities and differences between binge drinkers living in the UK and France. Alcohol drinking history and impulsivity ratings were recorded from seventy-one participants [(37 UK (Binge drinkers N = 19); 34 France (Binge drinkers N = 17)], who then underwent a neuroimaging study. During functional magnetic resonance imaging, participants viewed images of bodily pain (vs. no-pain), while adopting the perspective of self (pain recipient) or other (observer of someone else experiencing pain). Anterior midcingulate cortex (aMCC) and insula activation distinguished pain from no-pain conditions. Binge drinkers showed stronger regional neural activation than non-binge drinkers within a cluster spanning fusiform gyrus and inferior temporal gyrus, encompassing the Fusiform Body Area. Binge drinkers compared to non-binge drinkers also took longer to respond when viewing pictures depicting pain, in particular when adopting the perspective of self. Relationships between changes in brain activation and behavioural responses in pain versus no pain conditions (self or other perspective) indicated that whereas non-binge drinkers engage areas supporting self to other distinction, binge drinkers do not. Our findings suggest that alcohol binge drinking is associated with different empathy-related behavioral and brain responses, consistent with the proposed importance of empathy in the development of AUD.
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http://dx.doi.org/10.1016/j.nicl.2020.102322DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7338615PMC
June 2020

Brain-body interactions underlying the association of loneliness with mental and physical health.

Neurosci Biobehav Rev 2020 09 28;116:283-300. Epub 2020 Jun 28.

Department of Neuroscience, Brighton and Sussex Medical School (BSMS), University of Sussex, Falmer, BN1 9RY, UK; Sackler Centre for Consciousness Science, University of Sussex, Falmer, BN1 9RR, UK; Sussex Partnership NHS Foundation Trust, Brighton, BN2 3EW, UK.

Loneliness can be operationalized as the actual or perceived absence of those social relationships that serve to meet basic emotional needs. In contrast to solitude, a chosen state of being without company, loneliness is associated with negative affect and emotional distress. Loneliness can have detrimental effects on mental and physical wellbeing, expressed as an increased risk of morbidity and mortality. Higher rates of loneliness are observed in patients suffering from chronic health conditions, mental health conditions, cardiovascular problems, and neurodivergent populations, including autistic individuals. While the link between poor health and loneliness is established, the identification of relevant underlying mechanisms is a difficult endeavor. In this narrative review, we provide an overview of published research and related literature describing the manifold interactions between loneliness, affective symptomatology, neural and embodied processing relevant to physical health, mental health, and neurodiversity. We propose a framework that can inform the identification of psychophysiological mechanisms underlying the link between loneliness and affective symptomatology that may represent interventional targets to mitigate the associated cycle of biopsychosocial morbidity.
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http://dx.doi.org/10.1016/j.neubiorev.2020.06.015DOI Listing
September 2020

Mega-analysis methods in ENIGMA: The experience of the generalized anxiety disorder working group.

Hum Brain Mapp 2020 Jun 29. Epub 2020 Jun 29.

National Institute of Mental Health (NIMH), National Institutes of Health (NIH), Bethesda, Maryland, USA.

The ENIGMA group on Generalized Anxiety Disorder (ENIGMA-Anxiety/GAD) is part of a broader effort to investigate anxiety disorders using imaging and genetic data across multiple sites worldwide. The group is actively conducting a mega-analysis of a large number of brain structural scans. In this process, the group was confronted with many methodological challenges related to study planning and implementation, between-country transfer of subject-level data, quality control of a considerable amount of imaging data, and choices related to statistical methods and efficient use of resources. This report summarizes the background information and rationale for the various methodological decisions, as well as the approach taken to implement them. The goal is to document the approach and help guide other research groups working with large brain imaging data sets as they develop their own analytic pipelines for mega-analyses.
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http://dx.doi.org/10.1002/hbm.25096DOI Listing
June 2020

Spelling Errors and Shouting Capitalization Lead to Additive Penalties to Trustworthiness of Online Health Information: Randomized Experiment With Laypersons.

J Med Internet Res 2020 06 10;22(6):e15171. Epub 2020 Jun 10.

Department of Neuroscience, Brighton and Sussex Medical School, Brighton, United Kingdom.

Background: The written format and literacy competence of screen-based texts can interfere with the perceived trustworthiness of health information in online forums, independent of the semantic content. Unlike in professional content, the format in unmoderated forums can regularly hint at incivility, perceived as deliberate rudeness or casual disregard toward the reader, for example, through spelling errors and unnecessary emphatic capitalization of whole words (online shouting).

Objective: This study aimed to quantify the comparative effects of spelling errors and inappropriate capitalization on ratings of trustworthiness independently of lay insight and to determine whether these changes act synergistically or additively on the ratings.

Methods: In web-based experiments, 301 UK-recruited participants rated 36 randomized short stimulus excerpts (in the format of information from an unmoderated health forum about multiple sclerosis) for trustworthiness using a semantic differential slider. A total of 9 control excerpts were compared with matching error-containing excerpts. Each matching error-containing excerpt included 5 instances of misspelling, or 5 instances of inappropriate capitalization (shouting), or a combination of 5 misspelling plus 5 inappropriate capitalization errors. Data were analyzed in a linear mixed effects model.

Results: The mean trustworthiness ratings of the control excerpts ranged from 32.59 to 62.31 (rating scale 0-100). Compared with the control excerpts, excerpts containing only misspellings were rated as being 8.86 points less trustworthy, those containing inappropriate capitalization were rated as 6.41 points less trustworthy, and those containing the combination of misspelling and capitalization were rated as 14.33 points less trustworthy (P<.001 for all). Misspelling and inappropriate capitalization show an additive effect.

Conclusions: Distinct indicators of incivility independently and additively penalize the perceived trustworthiness of online text independently of lay insight, eliciting a medium effect size.
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http://dx.doi.org/10.2196/15171DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7315370PMC
June 2020

Trait and state interoceptive abnormalities are associated with dissociation and seizure frequency in patients with functional seizures.

Epilepsia 2020 06 5;61(6):1156-1165. Epub 2020 Jun 5.

Neurosciences Research Centre, St George's University of London, London, UK.

Objective: Dissociative traits represent a disturbance in selfhood that may predispose to, and trigger, functional seizures (FSs). The predictive representation and control of the internal physiological state of the body (interoception) are proposed to underpin the integrity of the sense of self ("minimal selfhood"). Therefore, discrepancies between objective and subjective aspects of interoception may relate to symptom expression in patients with FSs. Here, we tested whether individual differences in trait measures of interoception relate to dissociative symptoms, and whether state interoceptive deficits predict FS occurrence.

Methods: Forty-one participants with FSs and 30 controls completed questionnaire ratings of dissociation, and measures of (1) interoceptive accuracy (IA)-objective performance on heartbeat detection tasks; (2) trait interoceptive sensibility-subjective sensitivity to internal sensations (using the Porges Body Perception Questionnaire); and (3) state interoceptive sensibility-subjective trial-by-trial measures of confidence in heartbeat detection. Interoceptive trait prediction error (ITPE) was calculated from the discrepancy between IA and trait sensibility, and interoceptive state prediction error (ISPE) from the discrepancy between IA and state sensibility.

Results: Patients with FSs had significantly lower IA and greater trait interoceptive sensibility than healthy controls. ITPE was the strongest predictor of dissociation after controlling for trait anxiety and depression in a regression model. ISPE correlated significantly with FS frequency after controlling for state anxiety.

Significance: Patients with FSs have disturbances in interoceptive processing that predict both dissociative traits reflecting the disrupted integrity of self-representation, and the expression of FSs. These findings provide insight into the pathophysiology of functional neurological disorder, and could lead to novel diagnostic and therapeutic approaches.
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http://dx.doi.org/10.1111/epi.16532DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7737228PMC
June 2020

Word up - Experiential and neurocognitive evidence for associations between autistic symptomology and a preference for thinking in the form of words.

Cortex 2020 07 27;128:88-106. Epub 2020 Mar 27.

Department of Psychology, University of York, York, United Kingdom.

Autism symptomology has a profound impact on cognitive and affective functioning, yet we know relatively little about how it shapes patterns of ongoing thought. In an exploratory study in a large population of neurotypical individuals, we used experience sampling to characterise the relationship between ongoing cognition and self-reported autistic traits. We found that with increasing autistic symptom score, cognition was characterised by thinking more in words than images. Analysis of structural neuroimaging data found that autistic traits linked to social interaction were associated with greater cortical thickness in a region of lingual gyrus (LG) within the occipital cortex. Analysis of resting state functional neuroimaging data found autistic traits were associated with stronger connectivity between the LG and a region of motor cortex. Importantly, the strength of connectivity between the LG and motor cortex moderated the link between autistic symptoms and thinking in words: individuals showing higher connectivity showed a stronger association between autistic traits and thinking in words. Together we provide behavioural and neural evidence linking autistic traits to the tendency to think in words which may be rooted in underlying cortical organisation. These observations lay the groundwork for research into the form and content of self-generated thoughts in individuals with the established diagnosis of autism.
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http://dx.doi.org/10.1016/j.cortex.2020.02.019DOI Listing
July 2020

Impact of cardiac interoception cues and confidence on voluntary decisions to make or withhold action in an intentional inhibition task.

Sci Rep 2020 03 6;10(1):4184. Epub 2020 Mar 6.

Sackler Centre for Consciousness Science, University of Sussex, Brighton, UK.

Interoceptive signals concerning the internal physiological state of the body influence motivational feelings and action decisions. Cardiovascular arousal may facilitate inhibition to mitigate risks of impulsive actions. Baroreceptor discharge at ventricular systole underpins afferent signalling of cardiovascular arousal. In a modified Go/NoGo task, decisions to make or withhold actions on 'Choose' trials were not influenced by cardiac phase, nor individual differences in heart rate variability. However, cardiac interoceptive awareness and insight predicted how frequently participants chose to act, and their speed of action: Participants with better awareness and insight tended to withhold actions and respond slower, while those with poorer awareness and insight tended to execute actions and respond faster. Moreover, self-reported trait urgency correlated negatively with intentional inhibition rates. These findings suggest that lower insight into bodily signals is linked to urges to move the body, putatively by engendering noisier sensory input into motor decision processes eliciting reactive behaviour.
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http://dx.doi.org/10.1038/s41598-020-60405-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7060346PMC
March 2020

Can't get it off my brain: Meta-analysis of neuroimaging studies on perseverative cognition.

Psychiatry Res Neuroimaging 2020 01 21;295:111020. Epub 2019 Nov 21.

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

Perseverative cognition (i.e. rumination and worry) describes intrusive, uncontrollable, repetitive thoughts. These negative affective experiences are accompanied by physiological arousal, as if the individual were facing an external stressor. Perseverative cognition is a transdiagnostic symptom, yet studies of neural mechanisms are largely restricted to specific clinical populations (e.g. patients with major depression). The present study applied activation likelihood estimation (ALE) meta-analyses to 43 functional neuroimaging studies of perseverative cognition to elucidate the neurobiological substrates across individuals with and without psychopathological conditions. Task-related and resting state functional connectivity studies were examined in separate meta-analyses. Across task-based studies, perseverative cognition engaged medial frontal gyrus, cingulate gyrus, insula, and posterior cingulate cortex. Resting state functional connectivity studies similarly implicated posterior cingulate cortex together with thalamus and anterior cingulate cortex (ACC), yet the involvement of ACC distinguished between perseverative cognition in healthy controls (HC) and clinical groups. Perseverative cognition is accompanied by the engagement of prefrontal, insula and cingulate regions, whose interaction may support the characteristic conjunction of self-referential and affective processing with (aberrant) cognitive control and embodied (autonomic) arousal. Within this context, ACC engagement appears critical for the pathological expression of rumination and worry.
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http://dx.doi.org/10.1016/j.pscychresns.2019.111020DOI Listing
January 2020

Online psychotherapy: trailblazing digital healthcare.

BJPsych Bull 2020 Apr;44(2):60-66

Brighton and Sussex Medical School, UK.

Advances in digital technology have a profound impact on conventional healthcare systems. We examine the trailblazing use of online interventions to enable autonomous psychological care which can greatly enhance individual- and population-level access to services. There is strong evidence supporting online cognitive-behavioural therapy and more engaging programmes are now appearing so as to reduce user 'attrition'. The next generation of autonomous psychotherapy programmes will implement adaptive and personalised responses, moving beyond impersonalised advice on cognitive and behavioural techniques. This will be a more authentic form of psychotherapy that integrates therapy with the actual relationship experiences of the individual user.
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http://dx.doi.org/10.1192/bjb.2019.66DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7283124PMC
April 2020

Heart rate variability as a biomarker in health and affective disorders: A perspective on neuroimaging studies.

Neuroimage 2019 11 3;202:116072. Epub 2019 Aug 3.

Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, Falmer, BN1 9RY, UK; Sackler Centre for Consciousness Science, University of Sussex, Falmer, BN1 9RR, UK; Sussex Partnership NHS Foundation Trust, Brighton, BN2 3EW, UK.

The dynamic embodiment of psychological processes is evident in the association of health outcomes, behavioural traits and psychological functioning with Heart Rate Variability (HRV). The dominant high-frequency component of HRV is an index of the central neural control of heart rhythm, mediated via the parasympathetic vagus nerve. HRV provides a potential objective measure of action policies for the adaptive and predictive allostatic regulation of homeostasis within the cardiovascular system. In its support, a network of brain regions (referred to as the 'central autonomic network') maps internal state, and controls autonomic responses. This network includes regions of prefrontal cortex, anterior cingulate cortex, insula, amygdala, periaqueductal grey, pons and medulla. Human neuroimaging studies of neural activation and functional connectivity broadly endorse this architecture, and its link with cardiac regulation at rest and dysregulation in clinical states that include affective disorders. In this review, we appraise neuroimaging research and related evidence for HRV as an informative marker of autonomic integration with affect and cognition, taking a perspective on function and organisation. We consider evidence for the utility of HRV as a metric to inform targeted interventions to improve autonomic and affective dysregulation, and suggest research questions for further investigation.
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http://dx.doi.org/10.1016/j.neuroimage.2019.116072DOI Listing
November 2019

Effect of alcohol on the sense of agency in healthy humans.

Addict Biol 2020 07 20;25(4):e12796. Epub 2019 Jun 20.

Sussex Addiction Research and Intervention Centre (SARIC), School of Psychology, University of Sussex, Brighton, UK.

Even at low to moderate doses, ingestion of the widely used recreational drug alcohol (ethanol) can impact cognitive and emotional processing. Recent studies show that the sense of agency (SoA; ie, the subjective experience of voluntary control over actions) can be modulated by specific pharmacological manipulations. The SoA, as quantified by the intentional binding (IB) paradigm, is enhanced by direct or indirect dopaminergic agonists in patients with Parkinson's disease and by ketamine (an N-methyl-D-aspartate (NMDA) receptor antagonist) in healthy individuals. These findings implicate dopaminergic and glutamatergic neurotransmission in mechanisms underlying SoA. Alcohol has a complex set of actions, including disinhibition of dopaminergic neurotransmission and allosteric antagonism at NMDA receptors. Here, we tested the hypothesis that low to moderate doses of alcohol would enhance SoA, and impact impulsivity and subjective emotional state. We conducted two experiments in 59 healthy male and female social drinkers, who ingested either a placebo "vehicle," or one of two doses of ethanol: 0.4 and 0.6 g/kg. In both experiments, we observed increased SoA/IB at both doses of alcohol exposure, relative to the placebo condition. We found no correlation between the effects of alcohol on IB and on impulsivity or subjective emotional state. Our findings might have implications for social and legal responsibility related to alcohol use, particularly in states prior to overt intoxication. Further studies are necessary to investigate the effects of alcohol and other addictive substances on the SoA.
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http://dx.doi.org/10.1111/adb.12796DOI Listing
July 2020

Interoceptive awareness mitigates deficits in emotional prosody recognition in Autism.

Biol Psychol 2019 09 1;146:107711. Epub 2019 Jun 1.

Psychiatry, Brighton and Sussex Medical School, Falmer, BN1 9RR, UK; Neuroscience, Brighton and Sussex Medical School, BN1 9RR, UK; Sackler Centre for Consciousness Science, University of Sussex, Falmer, BN1 9RR, UK; Sussex Partnership NHS Foundation Trust, Brighton, BN2 3EW, UK.

The sensing of internal bodily signals, a process known as interoception, contributes to subjective emotional feeling states that can guide empathic understanding of the emotions of others. Individuals with Autism Spectrum Conditions (ASC) typically show an attenuated intuitive capacity to recognise and interpret other peoples' emotional signals. Here we test directly if differences in interoceptive processing relate to the ability to perceive emotional signals from the intonation of speech (affective prosody) in ASC adults. We employed a novel prosody paradigm to compare emotional prosody recognition in ASC individuals and a group of neurotypical controls. Then, in a larger group of ASC individuals, we tested how recognition of affective prosody related to objective, subjective and metacognitive (awareness) psychological dimensions of interoception. ASC individuals showed reduced recognition of affective prosody compared to controls. Deficits in performance on the prosody task were mitigated by greater interoceptive awareness, so that ASC individuals were better able to judge the prosodic emotion if they had better insight into their own interoceptive abilities. This data links the ability to access interoceptive representations consciously to the recognition of emotional expression in others, suggesting a crossmodal target for interventions to enhance interpersonal skills.
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http://dx.doi.org/10.1016/j.biopsycho.2019.05.011DOI Listing
September 2019

A Bayesian Account of the Sensory-Motor Interactions Underlying Symptoms of Tourette Syndrome.

Front Psychiatry 2019 5;10:29. Epub 2019 Mar 5.

Sackler Centre for Consciousness Science, University of Sussex, Brighton, United Kingdom.

Tourette syndrome is a hyperkinetic movement disorder. Characteristic features include tics, recurrent movements that are experienced as compulsive and "unwilled"; uncomfortable premonitory sensations that resolve through tic release; and often, the ability to suppress tics temporarily. We demonstrate how these symptoms and features can be understood in terms of aberrant predictive (Bayesian) processing in hierarchical neural systems, explaining specifically: why tics arise, their "unvoluntary" nature, how premonitory sensations emerge, and why tic suppression works-sometimes. In our model, premonitory sensations and tics are generated through over-precise priors for sensation and action within somatomotor regions of the striatum. Abnormally high precision of priors arises through the dysfunctional synaptic integration of cortical inputs. These priors for sensation and action are projected into primary sensory and motor areas, triggering premonitory sensations and tics, which in turn elicit prediction errors for unexpected feelings and movements. We propose experimental paradigms to validate this Bayesian account of tics. Our model integrates behavioural, neuroimaging, and computational approaches to provide mechanistic insight into the pathophysiological basis of Tourette syndrome.
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http://dx.doi.org/10.3389/fpsyt.2019.00029DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6412155PMC
March 2019

Response time as a proxy of ongoing mental state: A combined fMRI and pupillometry study in Generalized Anxiety Disorder.

Neuroimage 2019 05 21;191:380-391. Epub 2019 Feb 21.

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

In Generalized Anxiety Disorder (GAD), fluctuations in ongoing thoughts (i.e., mind-wandering) often take the form of rigid and intrusive perseverative cognition, such as worry. Here, we sought to characterise the neural correlates of mind-wandering and perseverative cognition, alongside autonomic nervous system indices of central arousal, notably pupil dilation. We implemented a protocol incorporating the dynamic delivery of thought-probes within a functional neuroimaging task. Sixteen individuals with GAD and sixteen matched healthy controls (HC) underwent functional magnetic resonance imaging with concomitant pupillometry. Participants performed a series of low-demand tracking tasks, responding to occasional changes in a target stimulus. Such a task is typically accompanied by self-generated, off-task thinking. Thought-probes were triggered based on an individual's response time (RT) when responding to the change in the target. Subjective reports showed that long RT predicted off-task thinking/mind-wandering. Moreover, long RT and mind-wandering were also associated with larger pupil diameter. This effect was exaggerated in GAD patients during perseverative cognition. Within brain, during both pre-target periods and target events, there were distinct neural correlates for mind-wandering (e.g., anterior cingulate and paracingulate activation at target onset) and perseverative cognition (e.g., opposite patterns of activation in posterior cingulate and cerebellum at target onset in HC and GAD). Results suggest that not only attention systems but also sensory-motor cortices are important during off-task states. Interestingly, changes across the 'default mode network' also tracked fluctuations in pupillary size. Autonomic expression in pupillary changes mirrors brain activation patterns that occur during different forms of repetitive thinking.
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http://dx.doi.org/10.1016/j.neuroimage.2019.02.038DOI Listing
May 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

Interoceptive accuracy predicts nonplanning trait impulsivity.

Psychophysiology 2019 06 31;56(6):e13339. Epub 2019 Jan 31.

Behavioural and Clinical Neuroscience, School of Psychology, University of Sussex, Brighton, United Kingdom.

Influential theories concerning personality argue that many impulsive individuals show physiological underarousal at rest. This interoceptive state is proposed to be egodystonic, motivating impulsive maladaptive actions to enhance arousal. However, there is little empirical research on this matter. The current study tested the relationship between physiological markers of arousal, measures of interoceptive (in)sensitivity, and trait impulsivity in a nonclinical sample of young adults. Experiment 1 investigated whether individuals (N = 31) with high trait impulsivity show decreased resting measures of arousal (indexed from heart rate, heart rate variability, and sympathetic electrodermal activity). Experiment 2 assessed whether trait impulsivity is linked to interoceptive abilities (N = 60). Overall, our results do not provide any compelling support for the underarousal theory of impulsivity. However, impaired interoceptive (cardiac discrimination) accuracy predicted the degree of Barratt nonplanning impulsivity, such that individuals with a better ability to distinguish between internal (bodily) and external signals manifest lower levels of nonplanning trait impulsivity. These findings open an avenue for potential novel interventions aimed at improving planning abilities via better interoceptive discrimination.
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http://dx.doi.org/10.1111/psyp.13339DOI Listing
June 2019

Pathophysiological and cognitive mechanisms of fatigue in multiple sclerosis.

J Neurol Neurosurg Psychiatry 2019 06 25;90(6):642-651. Epub 2019 Jan 25.

Translational Neuromodeling Unit (TNU), Institute for Biomedical Engineering, University of Zurich and ETH Zurich, Zurich, Switzerland.

Fatigue is one of the most common symptoms in multiple sclerosis (MS), with a major impact on patients' quality of life. Currently, treatment proceeds by trial and error with limited success, probably due to the presence of multiple different underlying mechanisms. Recent neuroscientific advances offer the potential to develop tools for differentiating these mechanisms in individual patients and ultimately provide a principled basis for treatment selection. However, development of these tools for differential diagnosis will require guidance by pathophysiological and cognitive theories that propose mechanisms which can be assessed in individual patients. This article provides an overview of contemporary pathophysiological theories of fatigue in MS and discusses how the mechanisms they propose may become measurable with emerging technologies and thus lay a foundation for future personalised treatments.
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http://dx.doi.org/10.1136/jnnp-2018-320050DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6581095PMC
June 2019

The impact of Yohimbine-induced arousal on facets of behavioural impulsivity.

Psychopharmacology (Berl) 2019 Jun 11;236(6):1783-1795. Epub 2019 Jan 11.

Behavioural and Clinical Neuroscience, School of Psychology, University of Sussex, Brighton, BN1 9QH, UK.

Rationale: State-dependent changes in physiological arousal may influence impulsive behaviours.

Objectives: To examine the relationship between arousal and impulsivity, we assessed the effects of yohimbine (an α-adrenergic receptor antagonist, which increases physiological arousal via noradrenaline release) on performance on established laboratory-based impulsivity measures in healthy volunteers.

Methods: Forty-three participants received a single dose of either yohimbine hydrochloride or placebo before completing a battery of impulsivity measures. Blood pressure and heart rate were monitored throughout the study.

Results: Participants in the yohimbine group showed higher blood pressure and better response inhibition in the Stop Signal Task, relative to the placebo group. Additionally, individual changes in blood pressure were associated with performance on Delay Discounting and Information Sampling tasks: raised blood pressure following drug ingestion was associated with more far-sighted decisions in the Delay Discounting Task (lower temporal impulsivity) yet reduced information gathering in the Information Sampling Task (increased reflection impulsivity).

Conclusions: These results support the notion that impulsive behaviour is dependent upon state physiological arousal; however, distinct facets of impulsivity are differentially affected by physiological changes.
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http://dx.doi.org/10.1007/s00213-018-5160-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6602985PMC
June 2019

Dimensions of interoception predict premonitory urges and tic severity in Tourette syndrome.

Psychiatry Res 2019 01 6;271:469-475. Epub 2018 Dec 6.

Sackler Centre for Consciousness Science, University of Sussex, University Kingdom; Department of Neuroscience, Brighton & Sussex Medical School, United Kingdom; Sussex Partnership NHS Foundation Trust, United Kingdom.

Interoceptive processes in Tourette syndrome may foster the premonitory urges that commonly precede tics. Twenty-one adults with TS and 22 controls completed heartbeat tracking and discrimination tasks. Three dimensions of interoception were examined: objective accuracy, metacognitive awareness, and subjective (self-report) sensibility. Trait interoceptive prediction error was calculated as the discrepancy between accuracy and sensibility. Participants with TS had numerically lower interoceptive accuracy on the heartbeat tracking task, and increased self-reported interoceptive sensibility. While these group differences were not significant, the discrepancy between lower interoceptive accuracy and heightened sensibility, i.e. the trait interoceptive prediction error, was significantly greater in TS compared to controls. This suggests a heightened higher-order sensitivity to bodily sensations in TS, relative to a noisier perceptual representation of afferent bodily signals. Moreover, interoceptive sensibility predicted the severity of premonitory sensations and tics. This suggests interventions that work to align dimensions of interoceptive experience in TS hold therapeutic potential.
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http://dx.doi.org/10.1016/j.psychres.2018.12.036DOI Listing
January 2019

Face perception enhances insula and motor network reactivity in Tourette syndrome.

Brain 2018 11;141(11):3249-3261

Sackler Centre for Consciousness Science, University of Sussex, UK.

Tourette syndrome is a neurodevelopmental disorder, characterized by motor and phonic tics. Tics are typically experienced as avolitional, compulsive, and associated with premonitory urges. They are exacerbated by stress and can be triggered by external stimuli, including social cues like the actions and facial expressions of others. Importantly, emotional social stimuli, with angry facial stimuli potentially the most potent social threat cue, also trigger behavioural reactions in healthy individuals, suggesting that such mechanisms may be particularly sensitive in people with Tourette syndrome. Twenty-one participants with Tourette syndrome and 21 healthy controls underwent functional MRI while viewing faces wearing either neutral or angry expressions to quantify group differences in neural activity associated with processing social information. Simultaneous video recordings of participants during neuroimaging enabled us to model confounding effects of tics on task-related responses to the processing of faces. In both Tourette syndrome and control participants, face stimuli evoked enhanced activation within canonical face perception regions, including the occipital face area and fusiform face area. However, the Tourette syndrome group showed additional responses within the anterior insula to both neutral and angry faces. Functional connectivity during face viewing was then examined in a series of psychophysiological interactions. In participants with Tourette syndrome, the insula showed functional connectivity with a set of cortical regions previously implicated in tic generation: the presupplementary motor area, premotor cortex, primary motor cortex, and the putamen. Furthermore, insula functional connectivity with the globus pallidus and thalamus varied in proportion to tic severity, while supplementary motor area connectivity varied in proportion to premonitory sensations, with insula connectivity to these regions increasing to a greater extent in patients with worse symptom severity. In addition, the occipital face area showed increased functional connectivity in Tourette syndrome participants with posterior cortical regions, including primary somatosensory cortex, and occipital face area connectivity with primary somatosensory and primary motor cortices varied in proportion to tic severity. There were no significant psychophysiological interactions in controls. These findings highlight a potential mechanism in Tourette syndrome through which heightened representation within insular cortex of embodied affective social information may impact the reactivity of subcortical motor pathways, supporting programmed motor actions that are causally implicated in tic generation. Medicinal and psychological therapies that focus on reducing insular hyper-reactivity to social stimuli may have potential benefit for tic reduction in people with Tourette syndrome.
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http://dx.doi.org/10.1093/brain/awy254DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6202569PMC
November 2018

Subjective embodiment during the rubber hand illusion predicts severity of premonitory sensations and tics in Tourette Syndrome.

Conscious Cogn 2018 10 15;65:368-377. Epub 2018 Oct 15.

Sackler Centre for Consciousness Science, University of Sussex, UK; Department of Neuroscience, Brighton & Sussex Medical School, UK; Sussex Partnership NHS Foundation Trust, UK.

In Tourette Syndrome, the expression of tics and commonly preceding premonitory sensations is associated with perturbed subjective feelings of self-control and agency. We compared responses to the Rubber Hand Illusion in 23 adults with TS and 22 controls. Both TS and control participants reported equivalent subjective embodiment of the artificial hand: feelings of ownership, location, and agency were greater during synchronous visuo-tactile stimulation, compared to asynchronous. However, individuals with TS did not manifest greater proprioceptive drift, an objective marker of embodiment observed in controls. An 'embodiment prediction error' index of the difference between subjective embodiment and objective proprioceptive drift correlated with severity of premonitory sensations. Feelings of ownership also correlated with premonitory sensation severity, and feelings of agency with tic severity. These findings suggest that subjective bodily ownership, as measured by the rubber hand illusion, contributes to susceptibility to the premonitory sensations that may be a precipitating factor in tics.
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http://dx.doi.org/10.1016/j.concog.2018.09.011DOI Listing
October 2018

Computerized Exposure Therapy for Spider Phobia: Effects of Cardiac Timing and Interoceptive Ability on Subjective and Behavioral Outcomes.

Psychosom Med 2019 01;81(1):90-99

From the Department of Neuroscience (Watson, Garfinkel, van Praag, Willmott, Wong, Meeten, Critchley), Trafford Centre for Medical Research, Brighton and Sussex Medical School, Brighton, United Kingdom; Sackler Centre for Consciousness Science (Garfinkel, van Praag, Critchley), University of Sussex, Brighton, United Kingdom; Institute of Psychiatry, Psychology and Neuroscience (Meeten), King's College London, London, United Kingdom; and Sussex Partnership NHS Foundation Trust (Critchley), Sussex Education Centre Millview, Hove, United Kingdom.

Objective: Spider phobia is a common form of anxiety disorder for which exposure therapy is an effective first-line treatment. Motivated by the observed modulation of threat processing by afferent cardiac signals, we tested the hypothesis that interoceptive information concerning cardiovascular arousal can influence the outcomes of computerized exposure therapy for spider phobia.

Method: Fifty-three normal healthy participants with high spider phobia scores underwent one of the following three modified computerized exposure protocols, defined by the timing of exposure to brief spider stimuli within the cardiac cycle: systole (during afferent baroreceptor firing); diastole (during baroreceptor-quiescent interbeat interval); random (noncontingent on cardiac cycle). Outcomes were judged on phobic and anxiety measures and physiological data (skin conductance). Individuals were also rated on interoceptive accuracy.

Results: MANCOVA analysis showed that timing group affected the outcome measures (F(10,80) = 2.405, p = .015) and there was a group interaction with interoception ability (F(15,110) = 1.808, p = .045). Subjective symptom reduction was greatest in the systolic group relative to the other two groups (diastolic (t = 3.115, ptukey = .009); random (t = 2.438, ptukey = .048)), with greatest reductions in those participants with lower interoceptive accuracy. Behavioral aversion reduced more in cardiac-contingent groups than the noncontingent (random) group (diastolic (t = 3.295, ptukey = .005); systolic (t = 2.602, ptukey = .032)). Physiological (skin conductance response) responses remained strongest for spider stimuli presented at cardiac systole.

Conclusions: Interoceptive information influences exposure benefit. The reduction in the subjective expression of fear/phobia is facilitated by "bottom-up" afferent signals, whereas improvement in the behavioral expression is further dependent on "top-down" representation of self-related physiology (heart rhythm). Individual interoceptive differences moderate these effects, suggesting means to personalize therapy.
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http://dx.doi.org/10.1097/PSY.0000000000000646DOI Listing
January 2019