Psychosomatics and psychopathology: looking up and down from the brain

doi:10.1016/j.psyneuen.2005.04.014

Psychoneuroendocrinology

Volume 30, Issue 10, November 2005, Pages 1050-1058

https://doi.org/10.1016/j.psyneuen.2005.04.014 Get rights and content

Summary

The autonomic nervous system (ANS) plays a role in a wide range of somatic and mental diseases. Using a model of neurovisceral integration, this article describes how autonomic imbalance and decreased parasympathetic tone in particular may be the final common pathway linking negative affective states and conditions to ill health. The central nervous system (CNS) network that regulates autonomic balance (central autonomic network, CAN) is closely related and partially overlaps with networks serving executive, social, affective, attentional, and motivated behavior (anterior executive region, AER; and Damasio's [Damasio, A.R., 1998. Emotion in the perspective of an integrated nervous system. Brain Res. Rev. 26, 83–86.] ‘emotion circuit’). A common reciprocal inhibitory cortico-subcortical neural circuit serves to regulate defensive behavior, including autonomic, emotional and cognitive features. This inhibitory cortico-subcortical circuit may structurally, as well as functionally, link psychological processes with health-related physiology. When the prefrontal cortex is taken ‘offline’ for whatever reason, parasympathetic inhibitory action is withdrawn and a relative sympathetic dominance associated with disinhibited defensive circuits is released, which can be pathogenic when sustained for long periods. This state is indicated by low heart rate variability (HRV), which is a marker for low parasympathetic activation and prefrontal hypoactivity. Consistent with this, HRV is associated with a range of psychological and somatic pathological conditions, including immune dysfunction. Finally, we discuss supportive evidence from recent studies of the reflexive startle blink, attention and working memory, which shows that low HRV predicts hypervigilance and inefficient allocation of attentional and cognitive resources.

Section snippets

The importance of inhibition

Importantly, like the heart, sympathoexcitatory subcortical threat circuits are under tonic inhibitory control by the prefrontal cortex (Amat et al., 2005, Thayer, in press). For example, the amygdala, which has outputs to autonomic, endocrine, and other physiological regulation systems, and becomes active during threat and uncertainty, is under tonic inhibitory control via GABAergic-mediated projections from the prefrontal cortex (Davidson, 2000, Thayer, in press). Thus the default response to

Vagal function, autonomic balance and disease

There are multiple measures that can be used to index activity of the vagus nerve. Resting HR, by virtue of its tonic inhibitory control via the vagus, is a simple, inexpensive, and non-invasive measure of vagal function and autonomic balance. The HR change following cessation of exercise is another measure that has been used to characterize vagal function. The decrease in HR after termination of exercise has been termed HR recovery and standardized methods have been developed for its

The central autonomic network

Investigators have identified functional units within the central nervous system (CNS) that support goal-directed behavior and adaptability. One such entity is the central autonomic network (CAN) (Benarroch, 1993, Benarroch, 1997). Functionally, this network is an integrated component of an internal regulation system through which the brain controls visceromotor, neuroendocrine, and behavioral responses that are critical for goal-directed behavior, adaptability, and health. Structurally, the

Autonomic regulation and prefrontal inhibition

We have argued above that autonomically mediated HRV is useful as an index of neurovisceral integration and organismic self-regulation. The interaction of sympathetic and parasympathetic outputs of the CAN at the sino-atrial node produces the complex beat-to-beat variability that marks a healthy, adaptive organism. Vagal activity dominates HR control, and thus HR is under tonic inhibitory vagal control (Levy, 1990, Uijtdehagge and Thayer, 2000). HRV is also associated with prefrontal cortex

Affective regulation

Affect regulation is a valuable skill that has clear implications for health. Emotions represent a distillation of an individual's perception of personally relevant environmental interactions, including not only challenges and threats but also the ability to respond to them (Frijda, 1988). Viewed as such, emotions reflect the integrity of one's ongoing adjustment to constantly changing environmental demands. When the affective system works properly, it promotes flexible adaptation to shifting

Attentional regulation and executive function

Attentional regulation and the ability to inhibit prepotent but inappropriate responses are also important for health in a complex environment. Many tasks important for survival in today's world involve cognitive functions such as working memory, sustained attention, behavioral inhibition, and general mental flexibility. These tasks are all associated with prefrontal cortical activity (Arnsten and Goldman-Rakic, 1998). Deficits in these cognitive functions are present in negative affective

Conclusion

Autonomic, cognitive, and affective regulation assist an organism in facing the challenge of an environment in constant flux. From a systems perspective, inhibitory processes can be viewed as negative feedback circuits that permit the interruption of ongoing behavior and redeployment of resources to other tasks. When these negative feedback mechanisms are compromised, positive feedback loops may develop as a result of disinhibition. These positive circuits can have disastrous consequences by

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Intolerance to psychological distress is associated with various forms of psychopathology, ranging from addiction to mood disturbance. The capacity to withstand aversive affective states is often explained by individual differences in cardiovagal tone as well as resting state connectivity of the ventromedial prefrontal cortex (vmPFC), a region involved in the regulation of emotions and cardio-autonomic tone. However, it is unclear which brain regions involved in distress tolerance show greater resting state functional connectivity (rsFC) as a function of resting heart rate variability (HRV).
One-hundred and twenty-six adults, aged 20 to 83.5 years, were selected from a lifespan cohort at the Nathan Kline Institute-Rockland Sample. Participants' distress tolerance levels were assessed based upon performance on the Behavioral Indicator of Resiliency to Distress (BIRD) task. Artifact-free resting-state functional brain scans collected during separate sessions were used. While inside the scanner, a pulse oximeter was used to record beat-to-beat intervals to derive high-frequency heart rate variability (HF-HRV). The relationship between HF-HRV and vmPFC to whole brain functional connectivity was compared between distress tolerant (BIRD completers) and distress intolerant (BIRD non-completers).
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In a lifespan sample of community-dwelling adults, distress tolerant individuals showed greater vmPFC connectivity with anterior and posterior hubs of the DMN compared to distress intolerant individuals. As a function of greater HF-HRV, distress tolerant individuals evidenced greater vmPFC with salience and executive control network hubs. These findings are consistent with deficits in neural resource allocation within a triple network resting amongst persons exhibiting behavioral intolerance to psychological distress.
Interpersonal touch and the importance of romantic partners for older adults’ neuroendocrine health
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Interpersonal touch is an essential aspect of human interaction that has the ability to regulate physiological stress responses. Prolonged exposure to stress can have cumulative multiphysiological effects; for example, allostatic load. Despite the increased susceptibility of social isolation for older adults, there is a paucity of research on the efficacy of touch in regulating stress responses among this population. It is also unknown whether touch confers benefits regardless of the person with whom it is shared. This study investigates the difference in physiological stress based on the frequency of touch (hugs, holding, or other close physical contact) shared with romantic partners as compared to other close adults (family, friends, and neighbours) in an older adult population. Data were analysed from 1419 respondents (aged 57–85 years) of the National Social Life, Health, and Aging Project (NSHAP) in 2005–2006. Principal components analysis determined whether the eight markers of allostatic load measured in the NSHAP function as a singular system or as distinct components. Analyses revealed three components of allostatic load: metabolic, cardiovascular, and neuroendocrine health. The results of multiple regression revealed that a higher frequency of interpersonal touch shared with romantic partners was associated with better neuroendocrine health (β = 0.13, p = 0.004) following adjustment for a variety of covariates (but not with better metabolic or cardiovascular health), with no associations apparent for touch from other close adults. These findings highlight the importance of promoting interpersonal touch with romantic partners for older adults’ neuroendocrine health.
Tonic and phasic cardiac vagal activity predict cognitive-affective processing in an emotional stop-signal task
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Both the Neurovisceral Integration Model and the Vagal Tank Theory propose cardiac vagal activity (CVA) as proxy for self-regulatory or processing resources required for attentional and top-down control as key mechanisms in executive functioning or emotion-regulation. These resources have, according to the Dual Competition Model, limited capacity and are prioritized for processing the most salient of different competing stimuli. As such, emotional and especially negative or threatening stimuli attract these self-regulatory/processing resources, and may thus interfere with ongoing cognitive processes if not integrated adaptively. Here, we investigated whether tonic and phasic CVA represent self-regulatory/processing resources and thus predict response inhibition in an emotional stop-signal task as a measure of cognitive-affective integration. Thereby, we examined not only the independent effects of tonic and phasic CVA, but whether and how the interaction of both variables predicts response inhibition. We assumed that the effects of CVA on response inhibition would be more pronounced in negatively-valenced trials compared to positive or neutral ones. Our results show that CVA significantly predicted response inhibition, with higher tonic CVA predicting faster, and larger phasic withdrawal CVA predicting slower stop-signal reaction times. The interactive effects of tonic and phasic CVA revealed that high tonic CVA levels prevented the negative effects of CVA withdrawal on response inhibition. Contrary to our assumption, we did not find differential effects of tonic and phasic CVA on trials with different valences. Our results support the notion of CVA as index for self-regulatory/processing resources. However, further research is needed to investigate how CVA is related to specific neural processes of cognitive-affective processing.
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An acute bout of exercise typically leads to short term exercise induced hypoalgesia (EIH), but this response is more variable in many chronic pain populations, including knee osteoarthritis (OA) and fibromyalgia (FM). There is evidence of autonomic nervous system (ANS) dysfunction in some chronic pain populations that may contribute to impaired EIH, but this has not been investigated in people with knee OA. The aim of this study was to assess the acute effects of isometric exercise on the nociceptive and autonomic nervous systems in people with knee OA and FM, compared to pain-free controls.
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Psychosomatics and psychopathology: looking up and down from the brain

Summary

Section snippets

The importance of inhibition

Vagal function, autonomic balance and disease

The central autonomic network

Autonomic regulation and prefrontal inhibition

Affective regulation

Attentional regulation and executive function

Conclusion

Electroencephalogr. Clin. Neurophysiol.

Mayo Clin. Proc.

Brain Res. Rev.

Prostaglandins Leukot. Essent.

J. Psychosom. Res.

Int. J. Psychophysiol.

Biol. Psychiatry

J. Anxiety Disord.

Trends Neurosci.

J. Affect. Disord.

Biol. Psychiatry

gender differences. Biol. Psychiatry

Prog. Neurobiol.

Prog. Brain Res.

Drug Alcohol Depend.

Heart rate and heart rate variability changes in the intracarotid sodium amobarbital (ISA) test

Epilepsia

Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus

Nat. Neurosci.

Noise stress impairs prefrontal cortical cognitive function in monkeys: evidence for a hyperdopaminergic mechanism

Arch. Gen. Psychiatr.

The central autonomic network

Autonomic imbalance, hypertension, and cardiovascular risk

Am. J. Hypertens.

Power spectral analysis of heart rate variability in psychiatry

Psychother. Psychosom.

The functional neuroanatomy of affective style

Contributions of anterior cingulate cortex to behavior

Brain

Age-associated increased interleukin-6 gene expression, late life diseases, and frailty

Annu. Rev. Med.

Anxiety and autonomic flexibility: a cardiovascular approach

Biol. Psychol.

The laws of emotion

Am. Psychol.

Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working memory tasks: implications for cortical and subcortical control of cardiac autonomic activity

Psychophysiology

The prefrontal landscape: implications of the functional architecture for understanding human mentation and the central executive

Reappraisal of heart rate as a risk factor in the general population

Eur. Heart J. Suppl.

Selective impairment in effortful information processing in major depression

J. Int. Neuropsychol. Soc.

Heart rate variability and its relation to prefrontal cognitive function: the effects of training and detraining

Eur. J. Appl. Physiol.

Contralateral EEG slowing and amobarbital distribution in Wada test: an intracarotid SPECT study

Epilepsia

Heart rate variability is inversely related to cortisol reactivity during cognitive stress

Psychosom. Med.

The normal range and determinants of the intrinsic heart rate in man

Cardiovasc. Res.

Emotions, morbidity, and mortality: new perspectives from psychoneuroimmunology

Annu. Rev. Psychol.