Mechanisms underlying the generation of autonomorespiratory coupling amongst the respiratory central pattern generator, sympathetic oscillators, and cardiovagal premotoneurons
The respiratory rhythm and pattern and sympathetic and parasympathetic outflows are generated by distinct, though overlapping, propriobulbar arrays of neuronal microcircuit oscillators constituting networks utilizing mutual excitatory and inhibitory neuronal interactions, residing principally within...
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| Format: | Article |
| Language: | English |
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IMR Press
2020-09-01
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| Series: | Journal of Integrative Neuroscience |
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| Online Access: | https://jin.imrpress.com/fileup/1757-448X/PDF/1601433308726-1616048374.pdf |
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| author | Michael G. Z. Ghali, George Zaki Ghali, Adriana Lima, Michael McDermott, Emma Glover, Stefanos Voglis, Jennifer Humphrey, Marton Skog Steinberger König, Henry Brem, Per Uhlén, Robert F. Spetzler, M. Gazi Yasargil |
| author_facet | Michael G. Z. Ghali, George Zaki Ghali, Adriana Lima, Michael McDermott, Emma Glover, Stefanos Voglis, Jennifer Humphrey, Marton Skog Steinberger König, Henry Brem, Per Uhlén, Robert F. Spetzler, M. Gazi Yasargil |
| author_sort | Michael G. Z. Ghali, George Zaki Ghali, Adriana Lima, Michael McDermott, Emma Glover, Stefanos Voglis, Jennifer Humphrey, Marton Skog Steinberger König, Henry Brem, Per Uhlén, Robert F. Spetzler, M. Gazi Yasargil |
| collection | DOAJ |
| description | The respiratory rhythm and pattern and sympathetic and parasympathetic outflows are generated by distinct, though overlapping, propriobulbar arrays of neuronal microcircuit oscillators constituting networks utilizing mutual excitatory and inhibitory neuronal interactions, residing principally within the metencephalon and myelencephalon, and modulated by synaptic influences from the cerebrum, thalamus, hypothalamus, cerebellum, and mesencephalon and ascending influences deriving from peripheral stimuli relayed by cranial nerve afferent axons. Though the respiratory and cardiovascular regulatory effector mechanisms utilize distinct generators, there exists significant overlap and interconnectivity amongst and between these oscillators and pathways, evidenced reciprocally by breathing modulation of sympathetic oscillations and sympathetic modulation of neural breathing. These coupling mechanisms are well-demonstrated coordinately in sympathetic- and respiratory-related central neuronal and efferent neurogram recordings and quantified by the findings of cross-correlation, spectra, and coherence analyses, combined with empirical interventions including lesioning and pharmacological agonist and antagonist microinjection studies, baroloading, barounloading, and hypoxic and/or hypercapnic peripheral and/or central chemoreceptor stimulation. Sympathetic and parasympathetic central neuronal and efferent neural discharge recordings evidence classic fast rhythms produced by propriobulbar neuronal networks located within the medullary division of the lateral tegmental field, coherent with cardiac sympathetic nerve discharge. These neural efferent nerve discharges coordinately evidence slow synchronous oscillations, constituted by Traube Hering (i.e., high frequency), Mayer wave (i.e., medium or low frequency), and vasogenic autorhythmicity (i.e., very low frequency) wave spectral bands. These oscillations contribute to coupling neural breathing, sympathetic oscillations, and parasympathetic cardiovagal premotoneuronal activity. The mechanisms underlying the origins of and coupling amongst, these waves remains to be unresolved. |
| first_indexed | 2024-04-13T08:07:20Z |
| format | Article |
| id | doaj.art-b95a323a08e745e0992fa2d41e7fac70 |
| institution | Directory Open Access Journal |
| issn | 1757-448X |
| language | English |
| last_indexed | 2024-04-13T08:07:20Z |
| publishDate | 2020-09-01 |
| publisher | IMR Press |
| record_format | Article |
| series | Journal of Integrative Neuroscience |
| spelling | doaj.art-b95a323a08e745e0992fa2d41e7fac702022-12-22T02:55:08ZengIMR PressJournal of Integrative Neuroscience1757-448X2020-09-0119352156010.31083/j.jin.2020.03.0196Mechanisms underlying the generation of autonomorespiratory coupling amongst the respiratory central pattern generator, sympathetic oscillators, and cardiovagal premotoneuronsMichael G. Z. Ghali, George Zaki Ghali, Adriana Lima, Michael McDermott, Emma Glover, Stefanos Voglis, Jennifer Humphrey, Marton Skog Steinberger König, Henry Brem, Per Uhlén, Robert F. Spetzler, M. Gazi Yasargil01Department of Neurological Surgery, Karolinska Institutet, Nobels väg 6 Solna and Alfred Nobels Allé 8 Huddinge SE-171 77, Stockholm, Sweden;2Department of Neurological Surgery, University of Helsinki, 00100, Helsinki, Finland;3Department of Neurological Surgery, University of Oslo, P.O. Box 1076 Blindern, N-0316 Oslo, Norway;4Department of Neurological Surgery, University of California San Francisco, 505 Parnassus Street, San Francisco, CA, 94143, USA;5Department of Neurological Surgery, Barrow Neurological Institute, 350 W. Thomas Road, Phoenix, Arizona, 85013, USA;6Department of Neurosurgery, University Hospital, Zurich, Rämistrasse Zurich, 100, 8091, Switzerland;7Purdue University, 610 University Mall, West Lafayette, IN, 47907, USA;8United States Environmental Protection Agency, 2777 Crystal Drive, Arlington, VA 22202;9Department of Neurological Surgery, University of Barcelona, Gran Via de les Corts Catalanes, Barcelona, 585 08007, Spain;10Department of Neurological Surgery, Oxford University, Oxford OX1, Oxford, United Kingdom;11Department of Neurological Surgery, Cambridge University, 184 Hills Road, Cambridge CB2 8PQ United Kingdom;12Department of Neurosurgery, Johns Hopkins Medical Institute, 1800 Orleans Street, Baltimore, MD 21287, USAThe respiratory rhythm and pattern and sympathetic and parasympathetic outflows are generated by distinct, though overlapping, propriobulbar arrays of neuronal microcircuit oscillators constituting networks utilizing mutual excitatory and inhibitory neuronal interactions, residing principally within the metencephalon and myelencephalon, and modulated by synaptic influences from the cerebrum, thalamus, hypothalamus, cerebellum, and mesencephalon and ascending influences deriving from peripheral stimuli relayed by cranial nerve afferent axons. Though the respiratory and cardiovascular regulatory effector mechanisms utilize distinct generators, there exists significant overlap and interconnectivity amongst and between these oscillators and pathways, evidenced reciprocally by breathing modulation of sympathetic oscillations and sympathetic modulation of neural breathing. These coupling mechanisms are well-demonstrated coordinately in sympathetic- and respiratory-related central neuronal and efferent neurogram recordings and quantified by the findings of cross-correlation, spectra, and coherence analyses, combined with empirical interventions including lesioning and pharmacological agonist and antagonist microinjection studies, baroloading, barounloading, and hypoxic and/or hypercapnic peripheral and/or central chemoreceptor stimulation. Sympathetic and parasympathetic central neuronal and efferent neural discharge recordings evidence classic fast rhythms produced by propriobulbar neuronal networks located within the medullary division of the lateral tegmental field, coherent with cardiac sympathetic nerve discharge. These neural efferent nerve discharges coordinately evidence slow synchronous oscillations, constituted by Traube Hering (i.e., high frequency), Mayer wave (i.e., medium or low frequency), and vasogenic autorhythmicity (i.e., very low frequency) wave spectral bands. These oscillations contribute to coupling neural breathing, sympathetic oscillations, and parasympathetic cardiovagal premotoneuronal activity. The mechanisms underlying the origins of and coupling amongst, these waves remains to be unresolved.https://jin.imrpress.com/fileup/1757-448X/PDF/1601433308726-1616048374.pdf|mechanisms|genesis|sympathorespiratory|coupling|modulation|cardiovagal|rostral ventrolateral medulla|sympathetic|hypercapnia|hypoxia |
| spellingShingle | Michael G. Z. Ghali, George Zaki Ghali, Adriana Lima, Michael McDermott, Emma Glover, Stefanos Voglis, Jennifer Humphrey, Marton Skog Steinberger König, Henry Brem, Per Uhlén, Robert F. Spetzler, M. Gazi Yasargil Mechanisms underlying the generation of autonomorespiratory coupling amongst the respiratory central pattern generator, sympathetic oscillators, and cardiovagal premotoneurons Journal of Integrative Neuroscience |mechanisms|genesis|sympathorespiratory|coupling|modulation|cardiovagal|rostral ventrolateral medulla|sympathetic|hypercapnia|hypoxia |
| title | Mechanisms underlying the generation of autonomorespiratory coupling amongst the respiratory central pattern generator, sympathetic oscillators, and cardiovagal premotoneurons |
| title_full | Mechanisms underlying the generation of autonomorespiratory coupling amongst the respiratory central pattern generator, sympathetic oscillators, and cardiovagal premotoneurons |
| title_fullStr | Mechanisms underlying the generation of autonomorespiratory coupling amongst the respiratory central pattern generator, sympathetic oscillators, and cardiovagal premotoneurons |
| title_full_unstemmed | Mechanisms underlying the generation of autonomorespiratory coupling amongst the respiratory central pattern generator, sympathetic oscillators, and cardiovagal premotoneurons |
| title_short | Mechanisms underlying the generation of autonomorespiratory coupling amongst the respiratory central pattern generator, sympathetic oscillators, and cardiovagal premotoneurons |
| title_sort | mechanisms underlying the generation of autonomorespiratory coupling amongst the respiratory central pattern generator sympathetic oscillators and cardiovagal premotoneurons |
| topic | |mechanisms|genesis|sympathorespiratory|coupling|modulation|cardiovagal|rostral ventrolateral medulla|sympathetic|hypercapnia|hypoxia |
| url | https://jin.imrpress.com/fileup/1757-448X/PDF/1601433308726-1616048374.pdf |
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