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      Differential cardiovascular responses to cutaneous afferent subtypes in a nociceptive intersegmental spinal reflex

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          Abstract

          Electrical stimulation to segmental dorsal cutaneous nerves (DCNs) activates a nociceptive sensorimotor reflex and the same afferent stimulation also evokes blood pressure (BP) and heart rate (HR) responses in rats. To investigate the relationship between those cardiovascular responses and the activation of nociceptive afferents, we analyzed BP and HR responses to electrical stimulations at each DCN from T6 to L1 at 0.5 mA to activate A-fiber alone or 5 mA to activate both A- and C-fibers at different frequencies. Evoked cardiovascular responses showed a decrease and then an increase in BP and an increase and then a plateau in HR. Segmentally, both cardiovascular responses tended to be larger when evoked from the more rostral DCNs. Stimulation frequency had a larger effect on cardiovascular responses than the rostrocaudal level of the DCN input. Stimulation strength showed a large effect on BP changes dependent on C-fibers whereas HR changes were dependent on A-fibers. Additional A-fiber activation by stimulating up to 4 adjacent DCNs concurrently, but only at 0.5 mA, affected HR but not BP. These data support that cutaneous nociceptive afferent subtypes preferentially contribute to different cardiovascular responses, A-fibers to HR and C-fibers to BP, with temporal (stimulation frequency) and spatial (rostrocaudal level) dynamics.

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          Most cited references38

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          Interoception: the sense of the physiological condition of the body.

          Converging evidence indicates that primates have a distinct cortical image of homeostatic afferent activity that reflects all aspects of the physiological condition of all tissues of the body. This interoceptive system, associated with autonomic motor control, is distinct from the exteroceptive system (cutaneous mechanoreception and proprioception) that guides somatic motor activity. The primary interoceptive representation in the dorsal posterior insula engenders distinct highly resolved feelings from the body that include pain, temperature, itch, sensual touch, muscular and visceral sensations, vasomotor activity, hunger, thirst, and 'air hunger'. In humans, a meta-representation of the primary interoceptive activity is engendered in the right anterior insula, which seems to provide the basis for the subjective image of the material self as a feeling (sentient) entity, that is, emotional awareness.
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            Autonomic dysreflexia.

            Autonomic dysreflexia (AD) may complicate spinal cord injured (SCI) subjects with a lesion level above the sixth thoracic level. There are several ways to remove triggering factors and, furthermore, new trigger mechanisms may be added by the introduction of new treatments. New data about the pathogenic mechanisms have been suggested in recent years as well as signs of metabolic effects associated with the reaction. This review of the syndrome includes clinical aspects of the AD reaction; the known pathogenic mechanisms, the incidence and prevalence and triggering factors. AD is associated with some cases of severe morbidity, including cerebral haemorrhage, seizures and pulmonary oedema. Symptomatic as well as specific treatments are discussed. Finally, some further questions are raised by the necessity of a proper definition of the syndrome, the revealing of the underlying pathophysiology, and new investigations concerning incidence and prevalence.
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              Differential control of sympathetic outflow.

              With advances in experimental techniques, the early views of the sympathetic nervous system as a monolithic effector activated globally in situations requiring a rapid and aggressive response to life-threatening danger have been eclipsed by an organizational model featuring an extensive array of functionally specific output channels that can be simultaneously activated or inhibited in combinations that result in the patterns of autonomic activity supporting behavior and mediating homeostatic reflexes. With this perspective, the defense response is but one of the many activational states of the central autonomic network. This review summarizes evidence for the existence of tissue-specific sympathetic output pathways, which are likely to include distinct populations of premotor neurons whose target specificity could be assessed using the functional fingerprints developed from characterizations of postganglionic efferents to known targets. The differential responses in sympathetic outflows to stimulation of reflex inputs suggest that the circuits regulating the activity of sympathetic premotor neurons must have parallel access to groups of premotor neurons controlling different functions but that these connections vary in their ability to influence different sympathetic outputs. Understanding the structural and physiological substrates antecedent to premotor neurons that mediate the differential control of sympathetic outflows, including those to noncardiovascular targets, represents a challenge to our current technical and analytic approaches.
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                Author and article information

                Contributors
                ktansey@mmrcrehab.org
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                13 December 2019
                13 December 2019
                2019
                : 9
                : 19049
                Affiliations
                [1 ]ISNI 0000 0001 0941 6502, GRID grid.189967.8, Departments of Neurology and Physiology, , Emory University, ; Atlanta, GA USA
                [2 ]ISNI 0000 0001 0941 6502, GRID grid.189967.8, Department of Biomedical Engineering, , Georgia Institute of Technology/Emory University, ; Atlanta, GA USA
                [3 ]ISNI 0000 0001 2097 4943, GRID grid.213917.f, School of Electrical and Computer Engineering, , Georgia Institute of Technology, ; Atlanta, GA USA
                [4 ]ISNI 0000 0004 0419 4084, GRID grid.414026.5, Spinal Cord Injury Clinic, Atlanta VA Medical Center, ; Atlanta, GA USA
                [5 ]ISNI 0000 0004 1937 0407, GRID grid.410721.1, Departments of Neurology, , University of Mississippi Medical Center, ; Jackson, MS USA
                [6 ]ISNI 0000 0004 1937 0407, GRID grid.410721.1, Departments of Neurobiology and Anatomical Sciences, , University of Mississippi Medical Center, ; Jackson, MS USA
                [7 ]ISNI 0000 0004 1937 0407, GRID grid.410721.1, Departments of Neurosurgery, , University of Mississippi Medical Center, ; Jackson, MS USA
                [8 ]ISNI 0000 0004 0419 9483, GRID grid.413879.0, G.V. (Sonny) Montgomery VA Medical Center, ; Jackson, MS USA
                [9 ]ISNI 0000 0004 0428 6210, GRID grid.419764.9, NeuroRobotics Lab, , Methodist Rehabilitation Center, ; Jackson, MS USA
                Author information
                http://orcid.org/0000-0002-6985-0690
                Article
                54072
                10.1038/s41598-019-54072-7
                6911054
                31836817
                078c5c64-4a8c-422d-ab1c-fd55940826f5
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 25 July 2019
                : 8 November 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000005, U.S. Department of Defense (United States Department of Defense);
                Award ID: W81XWH-10-1-0971
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                sensory processing,neurophysiology
                Uncategorized
                sensory processing, neurophysiology

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