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      Neurons in the dorsomedial medulla contribute to swallow pattern generation: Evidence of inspiratory activity during swallow

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          Abstract

          Active contraction of the diaphragm and other inspiratory pump muscles during swallow create a negative thoracic pressure to improve the movement of the bolus (food/liquid) into the esophagus. We tested the hypothesis that dorsomedial medullary inspiratory neurons, including the nucleus tractus solitarius (NTS, pre-motor to the phrenic) would be active during swallow induced by oral water infusion. We recorded neurons in the NTS and medial reticular formation in anesthetized spontaneously breathing cats, and induced swallow by injection of water into the oropharynx. Our results indicate that: 1) a majority of inspiratory cells in the dorsomedial medulla are active during swallow, 2) expiratory neurons are present in the medial reticular formation (deeper to the NTS) in unparalyzed cats and a majority of these cells decreased firing frequency during swallow. Our findings suggest that the dorsomedial medulla is a source of inspiratory motor drive during swallow and that a novel population of breathing-modulated neurons that also are modulated during swallowing exist in the medial reticular formation in unparalyzed animals.

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          Most cited references44

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          Analysis of pressure generation and bolus transit during pharyngeal swallowing.

          F McConnel (1987)
          Current pharyngeal deglutition theory has stressed the role of the pharyngeal constrictors as producing a peristaltic wave responsible for bolus propulsion through the pharynx. This thesis presents data obtained using manofluorography which supports the significance of tongue and laryngeal motion in swallowing. The usage of the term peristalsis to describe the constrictor contraction is challenged. The results of this quantitative study of swallowing in normal subjects, laryngectomized patients, and patients with restricted tongue motion show that tongue driving pressure and the negative pressure developed in the pharyngeal esophageal segment appear more important than the peristaltic-like pressure of the constrictors. Bolus transit is really dependent upon these two pressures. This model for analysis has clinical significance because it permits quantification of the pharyngeal swallowing mechanism.
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            A new bipolar electrode for electromyography

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              Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited.

              The currently accepted description of the pattern of electromyographic (EMG) activity in the pharyngeal swallow is that reported by Doty and Bosma in 1956; however, those authors describe high levels of intramuscle and of interindividual EMG variation. We reinvestigated this pattern, testing two hypotheses concerning EMG variation: 1) that it could be reduced with modern methodology and 2) that it could be explained by selective detection of different types of motor units. In eight decerebrate infant pigs, we elicited radiographically verified pharyngeal swallows and recorded EMG activity from a total of 16 muscles. Synchronization signals from the video-radiographic system allowed the EMG activity associated with each swallow to be aligned directly with epiglottal movement. The movements were highly stereotyped, but the recorded EMG signals were variable at both the intramuscle and interanimal level. During swallowing, some muscles subserved multiple functions and contained different task units; there were also intramuscle differences in EMG latencies. In this situation, statistical methods were essential to characterize the overall patterns of EMG activity. The statistically derived multimuscle pattern approximated to the classical description by Doty and Bosma (Doty RW, Bosma JF. J Neurophysiol 19: 44-60, 1956) with a leading complex of muscle activities. However, the mylohyoid was not active earlier than other muscles, and the geniohyoid muscle was not part of the leading complex. Some muscles, classically considered inactive, were active during the pharyngeal swallow.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draft
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: Project administrationRole: Writing – review & editing
                Role: Formal analysisRole: MethodologyRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: ValidationRole: Visualization
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: ValidationRole: Visualization
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Visualization
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: Supervision
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                19 July 2018
                2018
                : 13
                : 7
                : e0199903
                Affiliations
                [1 ] Department of Neurologic Surgery and Kentucky Spinal Cord Injury Research Center, College of Medicine, University of Louisville, Louisville, KY, United States of America
                [2 ] Department of Physiological Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL, United States of America
                [3 ] Comenius University in Bratislava, Jessenius Faculty of Medicine in Martin, Institute of Medical Biophysics, Martin, Slovak Republic
                The Research Center of Neurobiology-Neurophysiology of Marseille, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-9448-2175
                Article
                PONE-D-17-44734
                10.1371/journal.pone.0199903
                6053168
                30024913
                176a9b81-3591-4b14-8ea8-be56829d523e
                © 2018 Pitts et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 22 December 2017
                : 15 June 2018
                Page count
                Figures: 3, Tables: 3, Pages: 16
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 111215
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 109025
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 103415
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 131716
                Award Recipient :
                Research reported in this publication was supported by the Kentucky Spinal Cord and Head Injury Trust, The Commonwealth of Kentucky Challenge for Excellence, and the National Institute of Heart Lung and Blood of the National Institutes of Health under award R00HL111215; R01HL103415, R01HL109025, and R01HL131716. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
                Categories
                Research Article
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Ingestion
                Swallowing
                Medicine and Health Sciences
                Physiology
                Physiological Processes
                Ingestion
                Swallowing
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Respiration
                Breathing
                Medicine and Health Sciences
                Physiology
                Physiological Processes
                Respiration
                Breathing
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Motor Neurons
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
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                Motor Neurons
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                Anatomy
                Respiratory System
                Thoracic Diaphragm
                Medicine and Health Sciences
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                Respiratory System
                Thoracic Diaphragm
                Biology and Life Sciences
                Physiology
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                Membrane Potential
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                Membrane Potential
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                Neurophysiology
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                Biology and Life Sciences
                Organisms
                Eukaryota
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                Vertebrates
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                Cats
                Research and Analysis Methods
                Bioassays and Physiological Analysis
                Electrophysiological Techniques
                Muscle Electrophysiology
                Electromyography
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