Dissecting axes of autonomic control in humans: Insights from neuroimaging

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Abstract

The combination of functional brain imaging with measurement of peripheral autonomic responses in humans can provide insight into the embodiment of mental processes and the integration of cognition and emotion with changes in somatic physiology. Initial studies in healthy people and patents validate inferences from more detailed animal experiments regarding the organization of central autonomic control. In particular these have illustrated the coupling of behaviour with sympathetic arousal. Over the last two decades, the growth of emotional neuroscience alongside advances in functional brain imaging has fuelled investigations of relationships between perception, feeling states, somatic and autonomic bodily reactions. These studies have driven a more mechanistic understanding of brain systems through which bodily state is regulated and modified to support adaptive behaviour. In parallel, they have enabled the application of human neuroimaging to autonomic neuroscience. Specific methodological challenges are posed by combining physiological recordings with neuroimaging techniques, particularly functional magnetic resonance brain imaging, which are nevertheless addressable. Using such methods, the neural correlates of dynamic autonomic control has been systematically examined in studies of healthy individuals and patients with specific autonomic dysfunction (including autonomic failure, autonomic (neurally) mediated syncope and the postural tachycardia syndrome). These studies reveal antagonistic interaction of systems underpinning autonomic cardiovascular control (involving mid and subgenual cingulate cortices) and partial organ-specificity of other axes of autonomic response. Current and anticipated technical advances, including the integration of autonomically-focused microneurography and neural stimulation with advanced neuroimaging, will continue to provide detailed insight into dynamics of autonomic control. Translating these insights into clinical benefits remains a priority.

Section snippets

Application of brain imaging to autonomic neuroscience

Human functional neuroimaging can allow the measurement of dynamic changes in the activity of regions across the brain during behaviour. Neuroscientists, particularly psychologists, have capitalized on the opportunity to relate thoughts, perceptions, feelings and emotions to changes in the patterns of neural activity. This has resulted in an enhanced understanding of the coordinated working of the human brain, beyond knowledge gained from animal investigations and studies of neurological

Implementation of physiological recording within brain magnetic resonance imaging

The combination of autonomic monitoring (invasive or non-invasive) with functional magnetic resonance imaging (fMRI) offers a possibility to relate the neural dynamics of visceral regulation to patterns of activity within the brain at a time resolution broadly in keeping with these changes (the temporal resolution of fMRI is limited by the haemodynamic response to regional neural activity: the inflow of blood to an active region gives the blood oxygenation level dependent [BOLD] signal, which

Behaviourally-integrated physiology

Autonomic nervous control of internal bodily state is essential for adaptive behaviour, yet the models for understanding interaction between mind and body are relatively undeveloped within psychological literature. There is however a broad appreciation within animal learning that affective drive and motivational behaviour are grounded on physiological needs. Emotions can be encapsulated as hierarchical (social) elaborations, shaped by associative learning responses to rewards and punishments.

Correlational studies of the generation of peripheral autonomic responses

A first step to applying functional neuroimaging techniques to autonomic neuroscience is to see which brain regions are more active in states of ‘high arousal’; compared to ‘low arousal’. Clearly this strategy is already simplistic in conceptualization and raises confounds. Nevertheless, with appropriate control and qualified interpretation it has proved useful. One approach is to measure directly a physiological autonomic parameter [e.g. heart rate (King et al., 1999, Wager et al., 2009) blood

Brain activity related to representation of autonomic arousal states

A complementary line of neuroimaging research attempts to detail the representation of changes in internal state brought about through autonomic neural activity. This focus naturally extends to more general questions regarding the central neural representation of the visceral organs, a topic of study for fields of pain, gastroenterological, urological, cardiological and even immunological research (Craig, 2002, Critchley, 2009, Harrison et al., 2009). Valuable insights into the central pathways

Brain control of autonomic state: insights from patient studies

Studies of patients with selective disorders of the autonomic nervous system provide a means of testing and extending inferences obtained in healthy individuals. Such studies can provide fresh perspective on correlational data, and can have direct or indirect clinical value through enhancing our understanding of specific conditions. Neuroimaging studies of patients with peripheral autonomic denervation associated with pure autonomic failure (PAF) provide experimentally a valuable

Technical advances and future of neuroimaging of autonomic control

The above studies outline what can be achieved in the application of functional and structural neuroimaging to the delineation and dissection central autonomic control in healthy individuals and relevant patient group. The methods described are more or less standard, in terms of experimental design, non-invasive autonomic monitoring and imaging sequences. With the maturation of neuroimaging techniques and the broadening of their application, human autonomic neuroscience is becoming more

Summary

Functional neuroimaging, in combination with autonomic monitoring can provide dynamic information regarding the control of the autonomic nervous stem, with relevance to autonomic disorders and with broader implications for affective/cognitive neuroscience and psychosomatic medicine. Studies highlight the independent roles of dorsal anterior cingulate cortex and ventrolateral prefrontal/subgenual cortex in the behaviourally integrated generative control of cardiovascular response. In parallel,

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