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      Editorial: Integrity of the Autonomic Nervous System in Psychiatric and Neurological Disorders

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          Abstract

          The autonomic nervous system is an essential neural control network of the human body that maintains physiologic balance. It regulates function of vital systems such as the cardiovascular system, the gastrointestinal system, and the skin. Autonomic neuronal structures permeate and innervate the entire human organism, managing its autonomic functions largely independent from consciousness and thereby securing its survival. Professor Phillip Low, a pioneer of autonomic neurology, has once referred to the autonomic nervous system as the “Cinderella of Medicine,” a field of science, which attracted distinct interest in the scientific community but was limited by a substantial lack of coherent knowledge (1). When Low and a handful of out-of-the-box-thinking scientists such as Sir Roger Bannister from London, a famous neurologist and record-breaking middle-distance athlete, as well as David Robertson from Nashville, a distinguished neurologist and space physiologist, first embarked on the endeavor to explore the autonomic nervous system in the 1960s and 1970s, they could probably not foresee the future impact of their research. Nowadays, their observations provide a basis for diagnosis and treatment of highly prevalent and debilitating disorders, including metabolic disorders such as diabetes and neurodegenerative disorders such as Parkinson's disease. Over the past decades, techniques to assess structural and functional integrity of the autonomic nervous system have become paramount in understanding the pathophysiology of these diseases (2–4). Functional integrity of the sudomotor and cardiovascular autonomic nervous system can be tested non-invasively using well-established techniques such as quantitative sudomotor axon-reflex test, heart rate variability assessment and tilt table test (5). Structural integrity of the autonomic nervous system can be assessed using imaging of autonomic cerebral control centers such as the insular cortex as well as by immunohistochemical analysis of small nerve fibers in cutaneous punch biopsies (6, 7). Designing and further advancing these techniques helped improving our pathophysiological understanding of autonomic nervous system disorders and allowed identification of novel diagnostic and therapeutic targets. For example, Parkinson's disease has long been believed to be a primarily central synucleinopathy that affects brain regions of motor control. However, recent research has provided evidence that the peripheral autonomic nervous system is affected by deposition of misfolded alpha-synuclein long before motor control is clinically impaired. In these premotor disease stages the pathological form of alpha-synuclein can be detected in peripheral small autonomic nerve fibers of the skin, introducing a potential target for immunotherapy and other forms of targeted diagnostic and therapeutic approaches (8–10). As part of this article collection, Hong et al. reported an increased risk for atrial fibrillation in Parkinson's disease highlighting the significance of cardiac dysautonomia in these patients. In this population-based study in 15,434 newly diagnosed patients with Parkinson's disease, the authors observed a significant predictive association between atrial fibrillation and Parkinson's disease in premotor and early but not in later disease stages. This observation highlights the potential diagnostic value of atrial fibrillation in prodromal and early Parkinson's disease as well as the potential impact of cardiac dysautonomia on cardiovascular risk in these patients. While neurodegenerative synucleinopathies have recently been in the spotlight of autonomic neuroscience, autonomic dysfunction can in fact occur in a variety of neurological disorders such as diabetic or amyloidosis-related neuropathies, acute ischemic stroke, multiple sclerosis, neuroinflammatory diseases as well as psychiatric disorders such as anxiety and depression. This is of high clinical relevance as autonomic dysfunction can reduce quality of life, increase mortality, and increase cardiovascular risk. For example, autonomic impairment has been shown to independently increase mortality in patients with diabetic autonomic neuropathy and increase risk for cardiovascular disease in patients with depression (11, 12). Moreover, autonomic dysfunction seems to be associated with cognitive impairment as reported by Forte et al. in their systematic review, which is part of this article collection. In 20 studies comprising data from 19,431 study participants, they found that both increased sympathetic activity and decreased parasympathetic activity are associated with cognitive impairment. Notably, in the majority of included studies these associations were independent from demographic and clinical characteristics supporting a direct link between impairment of autonomic and cognitive functional integrity. Viewed in conjunction with the complex etiopathogenesis of autonomic dysfunction these observations highlight the need for personalized diagnostic and therapeutic strategies for disorders of the autonomic nervous system. Possible keys to improve early detection and personalized treatment of autonomic dysfunction comprise interdisciplinary symptom-driven clinical management strategies, advancement of assessment and further elucidation of the pathophysiological pathways leading to dysautonomia. Thus, interdisciplinary research on the autonomic nervous system has the potential to help improve quality of life, reduce mortality, and improve cardiovascular health. This would have implications for diseases that extend far beyond classic autonomic disorders such as diabetic neuropathy. Our article collection aims to provide a platform to foster autonomic neuroscience. Author Contributions TS drafted the first version of the manuscript. BM-W and KB revised the manuscript for intellectual content. Conflict of Interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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          Most cited references6

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          The Investigation of the Cardiovascular and Sudomotor Autonomic Nervous System—A Review

          The autonomic nervous system as operating system of the human organism permeats all organ systems with its pathways permeating that it is involved with virtually all diseases. Anatomically a central part, an afferent part and sympathetic and parasympathetic efferent system can be distinguished. Among the different functional subsystems of the autonomic nervous system, the cardiovascular autonomic nervous system is most frequently examined with easily recordable cardiovascular biosignals as heart rate and blood pressure. Although less widely established, sudomotor tests pose a useful supplement to cardiovascular autonomic assessment as impaired neurogenic sweating belongs to the earliest clinical signs of various autonomic neuropathies as well as neurodegenerative disorders and significantly reduces quality of life. Clinically at first, the autonomic nervous system is assessed with a detailed history of clinical autonomic function and a general clinical examination. As a lof of confounding factors can influence autonomic testing, subjects should be adequately prepared in a standardized way. Autonomic testing is usually performed in that way that the response of the autonomic nervous system to a well-defined challenge is recorded. As no single cardiovascular autonomic test is sufficiently reliable, it is recommended to use a combination of different approaches, an autonomic test battery including test to measure parasympathetic and sympathetic cardiovascular function (deep breathing test, Valsalva maneuver, tilt, or pressor test). More specialized tests include carotid sinus massage, assessment of baroreceptor reflex function, pharmacological tests or cardiac, and regional hemodynamic measurements. Techniques to measure functional integrity of sudomotor nerves include the quantitative sudomotor axon reflex sweat test, analysis of the sympathetic skin response as well as the thermoregulatory sweat test. In addition to these rather established techniques more recent developments have been introduced to reduce technical demands and interindividual variability such as the quantitative direct and indirect axon reflex testing or sudoscan. However, diagnostic accuracy of these tests remains to be determined. We reviewed the current literature on currently available autonomic cardiovascular and sudomotor tests with a focus on their physiological and technical mechanisms as well as their diagnostic value in the scientific and clinical setting.
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            Testing the autonomic nervous system.

            Diana Low (2003)
            Noninvasive, well-validated clinical tests of autonomic function are available and are in relatively wide use. These comprise an evaluation of sudomotor, cardiovagal, and adrenergic functions. These tests are very useful and have resulted in the recognition of milder degrees of autonomic failure and the presence of orthostatic intolerance that previously were missed. An extensive normative database and commercial equipment is available. The main limitations of the tests relate to the fact that they evaluate mainly the function of target tissues so that the status of autonomic reflexes are inferred. The tests can be affected by medications. There are more invasive, more time-consuming, or less validated tests of autonomic function that can directly record from sympathetic nerve fibers (microneurography) and mesenteric bed to study cerebral vasoregulation and the status of the veins.
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              Autonomic peripheral neuropathy.

              The autonomic neuropathies are a group of disorders in which the small, lightly myelinated and unmyelinated autonomic nerve fibres are selectively targeted. Autonomic features, which involve the cardiovascular, gastrointestinal, urogenital, sudomotor, and pupillomotor systems, occur in varying combination in these disorders. Diabetes is the most common cause of autonomic neuropathy in more developed countries. Autonomic neuropathies can also occur as a result of amyloid deposition, after acute infection, as part of a paraneoplastic syndrome, and after exposure to neurotoxins including therapeutic drugs. Certain antibodies (eg, anti-Hu and those directed against neuronal nicotinic acetylcholine receptor) are associated with autonomic signs and symptoms. There are several familial autonomic neuropathies with autosomal dominant, autosomal recessive, or X-linked patterns of inheritance. Autonomic dysfunction can occur in association with specific infections. The availability of sensitive and reproducible measures of autonomic function has improved physicians' ability to diagnose these disorders.
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                Author and article information

                Contributors
                Journal
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                1664-2295
                25 February 2020
                2020
                : 11
                : 138
                Affiliations
                [1] 1Department of Neurology, University Hospital Carl Gustav Carus, Technische Universität Dresden , Dresden, Germany
                [2] 2Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School , Boston, MA, United States
                Author notes

                Edited and reviewed by: Vaughan G. Macefield, Baker Heart and Diabetes Institute, Australia

                *Correspondence: Timo Siepmann timo.siepmann@ 123456ukdd.de

                This article was submitted to Autonomic Neuroscience, a section of the journal Frontiers in Neurology

                Article
                10.3389/fneur.2020.00138
                7052382
                a8b2ccbc-d6ae-461b-a5b0-fef44c1176fa
                Copyright © 2020 Siepmann, Min-Woo Illigens and Barlinn.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 11 December 2019
                : 07 February 2020
                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 12, Pages: 2, Words: 1381
                Categories
                Neurology
                Editorial

                Neurology
                autonomic,psychiatry,neurology,assessment,treatment
                Neurology
                autonomic, psychiatry, neurology, assessment, treatment

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