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      Vertebrate Evolution Conserves Hindbrain Circuits despite Diverse Feeding and Breathing Modes

      review-article
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      eNeuro
      Society for Neuroscience
      breathing, central rhythm generator, evolution, feeding, hindbrain

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          Abstract

          Feeding and breathing are two functions vital to the survival of all vertebrate species. Throughout the evolution, vertebrates living in different environments have evolved drastically different modes of feeding and breathing through using diversified orofacial and pharyngeal (oropharyngeal) muscles. The oropharyngeal structures are controlled by hindbrain neural circuits. The developing hindbrain shares strikingly conserved organizations and gene expression patterns across vertebrates, thus begs the question of how a highly conserved hindbrain generates circuits subserving diverse feeding/breathing patterns. In this review, we summarize major modes of feeding and breathing and principles underlying their coordination in many vertebrate species. We provide a hypothesis for the existence of a common hindbrain circuit at the phylotypic embryonic stage controlling oropharyngeal movements that is shared across vertebrate species; and reconfiguration and repurposing of this conserved circuit give rise to more complex behaviors in adult higher vertebrates.

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          Most cited references155

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          Breathing matters

          Breathing is a well-described, vital and surprisingly complex behaviour, with behavioural and physiological outputs that are easy to directly measure. Key neural elements for generating breathing pattern are distinct, compact and form a network amenable to detailed interrogation, promising the imminent discovery of molecular, cellular, synaptic and network mechanisms that give rise to the behaviour. Coupled oscillatory microcircuits make up the rhythmic core of the breathing network. Primary among these is the preBötzinger Complex (preBötC), which is composed of excitatory rhythmogenic interneurons and excitatory and inhibitory pattern-forming interneurons that together produce the essential periodic drive for inspiration. The preBötC coordinates all phases of the breathing cycle, coordinates breathing with orofacial behaviours and strongly influences, and is influenced by, emotion and cognition. Here, we review progress towards cracking the inner workings of this vital core.
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            Compartments and their boundaries in vertebrate brain development.

            Fifteen years ago, cell lineage restriction boundaries were discovered in the embryonic vertebrate hindbrain, subdividing it into a series of cell-tight compartments (known as rhombomeres). Compartition, together with segmentally reiterative neuronal architecture and the nested expression of Hox genes, indicates that the hindbrain has a truly metameric organization. This finding initiated a search for compartments in other regions of the developing brain. The results of recent studies have clarified where compartment boundaries exist, have shed light on molecular mechanisms that underlie their formation and have revealed an important function of these boundaries: the positioning and stabilization of local signalling centres.
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              Neurophysiology of swallowing.

              Swallowing is a complex motor event that is difficult to investigate in man by neurophysiological experiments. For this reason, the characteristics of the brain stem pathways have been studied in experimental animals. However, the sequential and orderly activation of the swallowing muscles with the monitoring of the laryngeal excursion can be recorded during deglutition. Although influenced by the sensory and cortical inputs, the sequential muscle activation does not alter from the perioral muscles caudally to the cricopharyngeal sphincter muscle. This is one evidence for the existence of the central pattern generator for human swallowing. The brain stem swallowing network includes the nucleus tractus solitarius and nucleus ambiguus with the reticular formation linking synaptically to cranial motoneuron pools bilaterally. Under normal function, the brain stem swallowing network receives descending inputs from the cerebral cortex. The cortex may trigger deglutition and modulate the brain stem sequential activity. The voluntarily initiated pharyngeal swallow involves several cortical and subcortical pathways. The interactions of regions above the brain stem and the brain stem swallowing network is, at present, not fully understood, particularly in humans. Functional neuroimaging methods were recently introduced into the human swallowing research. It has been shown that volitional swallowing is represented in the multiple cortical regions bilaterally but asymmetrically. Cortical organisation of swallowing can be continuously changed by the continual modulatory ascending sensory input with descending motor output. Dysphagia is a severe symptom complex that can be life threatening in a considerable number of patients. Three-fourths of oropharyngeal dysphagia is caused by neurological diseases. Thus, the responsibility of the clinical neurologist and neurophysiologist in the care for the dysphagic patients is twofold. First, we should be more acquainted with the physiology of swallowing and its disorders, in order to care for the dysphagic patients successfully. Second, we need to evaluate the dysphagic problems objectively using practical electromyography methods for the patients' management. Cortical and subcortical functional imaging studies are also important to accumulate more data in order to get more information and in turn to develop new and effective treatment strategies for dysphagic patients.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                10 March 2021
                16 April 2021
                Mar-Apr 2021
                : 8
                : 2
                : ENEURO.0435-20.2021
                Affiliations
                [1]Department of Neurobiology, Duke University , Durham, NC 27710
                Author notes

                The authors declare no competing financial interests.

                Author contributions: S.L. and F.W. wrote the paper.

                This work was supported by a subcontract for the National Institutes of Health Grant U19NS107466.

                F. Wang’s present address: McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139.

                Correspondence should be addressed to Fan Wang at fan_wang@ 123456mit.edu .
                Author information
                https://orcid.org/0000-0002-8580-3843
                https://orcid.org/0000-0003-2988-0614
                Article
                eN-REV-0435-20
                10.1523/ENEURO.0435-20.2021
                8174041
                33707205
                aaac86cd-4769-4419-9bb8-b53a30edaacc
                Copyright © 2021 Li and Wang

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 8 October 2020
                : 8 January 2021
                : 12 January 2021
                Page count
                Figures: 3, Tables: 3, Equations: 0, References: 155, Pages: 15, Words: 00
                Funding
                Funded by: http://doi.org/10.13039/100000065HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
                Award ID: U19NS107466
                Categories
                0675
                8
                Review
                Sensory and Motor Systems
                Custom metadata
                March/April 2021

                breathing,central rhythm generator,evolution,feeding,hindbrain

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