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• W2073648380 abstract "POINT-COUNTERPOINTCounterpoint: Medullary Pacemaker Neurons are Essential for Gasping, but not Eupnea, in MammalsJulian F. R. Paton, and Walter M. St.-JohnJulian F. R. Paton, and Walter M. St.-JohnPublished Online:01 Aug 2007https://doi.org/10.1152/japplphysiol.00003.2007aMoreSectionsPDF (87 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInEmail For more than 80 years, the brain stem mechanisms that might underlie the neurogenesis of automatic ventilatory activity have been debated. Mechanisms proposed have included the discharge of pacemaker neurons, inhibitory synaptic interactions within a neuronal circuit, or a combination of these processes. Inherent to these discussions has been the question as to whether there are state-dependent changes in the mechanisms for respiratory rhythm generation such as occur during the transition from eupnea to gasping.Eupnea and gasping differ in multiple aspects, with a primary difference being the rate of rise of inspiratory motor activity. In eupnea, phrenic activity increases gradually. In gasping, phrenic discharge reaches a peak almost immediately after onset and has a decrementing pattern (Fig. 1). During gasping, the temporal dispersion of cranial (X and XIIth nerves) vs. spinal motor outflows is lost as they synchronize, and laryngeal adductor activity (post-inspiratory discharge) is abolished (12, 19–21, 29; Fig 1). Therefore, we propose that multiple, simultaneously recorded motor outflows are necessary to assign behavioral terms to respiratory motor patterns.Fig. 1.Defining respiratory motor patterns. To describe patterns of respiratory activity, we propose that multiple motor outputs are recorded simultaneously in an attempt to characterize accurately patterns. Above are simultaneous recordings of integrated phrenic (PN), central vagus (cVN), and hypoglossal (XII) activities showing 2 types of respiratory output. The eupneic-like pattern consists of ramp inspiratory activity (all nerves), postinspiration (arrows, cVN) with XII exhibiting preinspiratory activity relative to PN (arrows). Exposure to hypoxia produces a decrementing pattern (all nerves) loss of postinspiration (cVN) and synchronization of cranial and spinal outflows; the latter is typical of gasping. Recordings made from an in situ arterially perfused juvenile rat preparation (12).Download figureDownload PowerPointRhythms in vitro.Although an in vitro en bloc preparation was introduced more than 20 years ago (26) and slice preparations soon thereafter (17), the rhythms generated by these in vitro preparations remain poorly defined. For en bloc preparations of the neonatal rat, the discharges of its cranial and spinal nerves have a similar invariant decrementing pattern that is initiated coincidentally and contains little post-inspiratory discharge (15–17).As en bloc preparations, activity recorded from the hypoglossal nerve of slice preparations from neonatal rats and mice can have a decrementing discharge (2, 3, 16, 17). Some continue to opine that this decrementing pattern represents a variant of eupnea (6) and that age and state-dependent changes account for the difference between the incrementing neural discharge, recorded in neonatal and adult in vivo and in situ preparations and the decrementing discharges of en bloc and slice preparations. However, other work indicates fundamentally similar respiratory patterns in immature and mature rats (4, 7, 21, 24, 29).Another confounding finding is that, in addition to the decrementing pattern, two other rhythmic patterns have been described for thick in vitro slices obtained from the medulla of mouse (9, 13, 27, 28). The reason for multiple rhythms from thick slices and a single rhythm from thin (350 μm) sections from the neonatal rat is unclear. However, thin sections are largely limited to the medullary “pre-Bötzinger complex,” the region for rhythm generation in vitro, whereas thick slices probably include other varying amounts of the ventral medullary respiratory column and are therefore different and cannot be compared easily.Neurogenesis of gasping by medullary pacemakers.Since the work of Lumsden in 1923 (10), the concept that gasping is generated by mechanisms intrinsic to the medulla has been well accepted. We acknowledge that the medulla can also generate “non-gasping” rhythms, but the mechanisms and physiological relevance of these elude us at present.Gasping is irreversibly eliminated following ablations in either the “gasping center” of the lateral tegemental field or the adjoining pre-Bötzinger complex. Both regions contain elements of the same neurons (18, 20).In eupnea, neurons in the pre-Bötzinger complex discharge during neural inspiration, expiration, or across both phases. In hypoxia-induced gasping, a subset of neurons begin to discharge in late neural expiration, prior to onset of the phrenic burst (12, 23). Some of these “pre-inspiratory” neuronal activities have the capacity for intrinsic rhythmic bursting that continues following a blockade of fast inhibitory and excitatory synaptic transmission. These rhythmic bursts, as well as gasping of in situ and in vivo preparations, are eliminated by blockers of persistent sodium channels (23). Similar burster neurons that are sensitive to riluzole have been identified in the pre-Bötzinger complex in vitro (13, 27).In vitro rhythms and gasping of in situ preparations are little altered by a blockade of inhibitory synaptic transmission, which is consistent with the hypothesis that the discharge of intrinsic bursting neurons may be essential for both rhythms (22). In contrast, a similar blockade markedly distorts eupnea of in vivo or in situ preparations, implying that inhibitory neuronal circuits are critical for this rhythm to be expressed (8, 11, 22).Neurogenesis of eupnea by intrinsically bursting neurons?A more fundamental question than whether the discharge of medullary burster neurons can generate eupnea is whether medullary mechanisms alone, be they pacemakers or a neuronal circuit, can generate eupnea.If eupnea is generated by the discharge of medullary bursters, a number of criteria must be fulfilled. First, a unique region that is critical for the neurogenesis of eupnea must be identified. Although ablation of many brain stem regions distorts eupnea, no region has been identified as a “noeud vital” for the neurogenesis of eupnea (20, 21, 24). Likewise, optical recordings of respiratory neuronal activities in a fetal mouse preparation failed to identify a specific medullary region in which the respiratory rhythm commenced (5).A second criterion is that blockers of intrinsic burster neurons should eliminate eupnea. One group of these is dependent on conductance through persistent sodium channels, with blockers of these channels eliminating some in vitro rhythms and hypoxia-induced gasping in vivo and in situ (13, 27). Also eliminated was a “non-gasping” rhythm of an in situ preparation having a brain stem transection at the pontomedullary junction (14). This non-gasping rhythm differs dramatically from eupnea recorded in a preparation having an intact pons because there is a marked alteration in the shape and amplitude of the inspiratory burst as well as a loss of postinspiratory discharge (1, 24, 25). For in situ preparations having an intact pons or in conscious rats, blockade of persistent sodium channels did not eliminate eupnea (25).Parenthetically, evaluations following brain stem transections are leading to additional confusion in that all non-gasping medullary rhythms are proposed to be variants of eupnea (6, 14). This proposal is premature and probably incorrect as shown by the differences in motor patterns and the response of medullary rhythms and pontomedullary rhythms to blockers of persistent sodium channels.A second group of intrinsic bursters, dependent on a conductance through calcium channels, has been identified using thick slice in vitro preparations of neonatal mouse (13, 27, 28). Neurons with similar characteristics have not yet been recorded in situ or in vivo.Finally, some laboratories rejected an essential role for any pacemakers even in the genesis of in vitro rhythms (2, 3, 6). This conclusion is based on the observation that an in vitro rhythm activity can be restored following a blockade of pacemaker discharge involving both persistent sodium and calcium conductances. Respiratory rhythm generation is considered to result from interactions among neurons in a localized medullary neuronal circuit. The nature of rhythm generation by this circuit is undefined. Synaptic inhibition is only considered essential for coordination with another medullary region in which expiratory activities are generated independent of those generating inspiratory discharge. Others consider that the in vitro rhythms that can be induced following a blockade of pacemaker discharge are not related to either the neurogenesis of eupnea or gasping (28).In summary, a critical problem is determining what the rhythms generated in vitro actually are and how they relate to adequately defined motor behaviors (e.g., eupnea, gasping) in vivo and in situ. Differences between in vitro findings, compared with those in vivo or in situ, may not reflect “plasticity” or “transformations” but rather fundamentally different mechanisms of rhythm generation.REFERENCES1 Abdala APL, Smith JC, Rybak IA, Paton JFR. Changes in the pattern of spinal and cranial respiratory motor outflows after micro, transverse sectioning of the pons in situ. Proc Physiol Soc 3: PC87, 2006.Google Scholar2 Del Negro CA, Morgado-Valle C, Feldman JL. Respiratory rhythm: an emergent network property? Neuron 34: 821–830, 2002.Crossref | PubMed | ISI | Google Scholar3 Del Negro CA, Morgado-Valle C, Hayes JA, Mackay DD, Pace RW, Crowder EA, Feldman JL. Sodium and calcium current-mediated pacemaker neurons and respiratory rhythm generation. J Neurosci 25: 446–453, 2005.Crossref | PubMed | ISI | Google Scholar4 Dutschmann M, Wilson RJA, Paton JFR. Respiratory activity in neonatal rats. 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J Physiol 490: 277–292, 1996.Crossref | PubMed | ISI | Google Scholar Previous Back to Top Next FiguresReferencesRelatedInformationCited ByKinetic properties of persistent Na+ current orchestrate oscillatory bursting in respiratory neurons9 October 2018 | Journal of General Physiology, Vol. 150, No. 11Defining the Rhythmogenic Elements of Mammalian BreathingJan-Marino Ramirez and Nathan Baertsch15 August 2018 | Physiology, Vol. 33, No. 5Inhalation broncho-pulmonaire de matières cérébrales et cartilagineuses au cours d’une respiration agoniqueAnnales de Pathologie, Vol. 34, No. 6The Cellular Building Blocks of Breathing1 October 2012Age-related changes in nitroxidergic neurons in some nuclei of rat medulla oblongata4 August 2010 | Russian Journal of Developmental Biology, Vol. 41, No. 4Degeneracy as a substrate for respiratory regulationRespiratory Physiology & Neurobiology, Vol. 172, No. 1-2Mylohyoid discharge of the in situ rat: a probe of pontile respiratory activities in eupnea and gaspingWalter M. St.-John, Alison H. Rudkin, and J. C. Leiter1 March 2010 | Journal of Applied Physiology, Vol. 108, No. 3Neuronal network properties underlying the generation of gaspingClinical and Experimental Pharmacology and Physiology, Vol. 36, No. 12Noeud vital for breathing in the brainstem: gasping—yes, eupnoea—doubtful12 September 2009 | Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 364, No. 1529Discharge of the hypoglossal nerve cannot distinguish eupnea from gasping, as defined by phrenic discharge, in the in situ mouseWalter M. St. John and J. C. Leiter1 September 2009 | Journal of Applied Physiology, Vol. 107, No. 3Genesis of gasping is independent of levels of serotonin in the Pet-1 knockout mouseWalter M. St.-John, Aihua Li, and J. C. Leiter1 September 2009 | Journal of Applied Physiology, Vol. 107, No. 3Structure–function analysis of rhythmogenic inspiratory pre-Bötzinger complex networks in “calibrated” newborn rat brainstem slicesRespiratory Physiology & Neurobiology, Vol. 168, No. 1-2Location and properties of respiratory neurones with putative intrinsic bursting properties in the rat in situ30 June 2009 | The Journal of Physiology, Vol. 587, No. 13Reconfiguration of the Pontomedullary Respiratory Network: A Computational Modeling Study With Coordinated In Vivo ExperimentsI. A. Rybak, R. O'Connor, A. Ross, N. A. Shevtsova, S. C. Nuding, L. S. Segers, R. Shannon, T. E. Dick, W. L. Dunin-Barkowski, J. M. Orem, I. C. Solomon, K. F. Morris, and B. G. Lindsey1 October 2008 | Journal of Neurophysiology, Vol. 100, No. 4Reconfiguration of respiratory-related population activity in a rostrally tilted transversal slice preparation following blockade of inhibitory neurotransmission in neonatal rats6 May 2008 | Pflügers Archiv - European Journal of Physiology, Vol. 457, No. 1Brain-derived neurotrophic factor enhances fetal respiratory rhythm frequency in the mouse preBötzinger complex in vitroEuropean Journal of Neuroscience, Vol. 28, No. 3Respiratory Control in Neonatal Rats Exposed to Prenatal Cigarette SmokeAmerican Journal of Respiratory and Critical Care Medicine, Vol. 177, No. 11Maintenance of gasping and restoration of eupnea after hypoxia is impaired following blockers of α1-adrenergic receptors and serotonin 5-HT2 receptorsWalter M. St.-John, and J. C. Leiter1 March 2008 | Journal of Applied Physiology, Vol. 104, No. 3ATP sensitivity of preBötzinger complex neurones in neonatal rat in vitro : mechanism underlying a P2 receptor-mediated increase in inspiratory frequency29 February 2008 | The Journal of Physiology, Vol. 586, No. 5Maternal drinking of alcohol: the newborn has the worst hangover29 February 2008 | The Journal of Physiology, Vol. 586, No. 5Eupnea of in situ rats persists following blockers of in vitro pacemaker burster activitiesRespiratory Physiology & Neurobiology, Vol. 160, No. 3 More from this issue > Volume 103Issue 2August 2007Pages 718-720 Copyright & PermissionsCopyright © 2007 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.00003.2007aPubMed17666729History Published online 1 August 2007 Published in print 1 August 2007 PDF download Metrics Downloaded 232 times" @default.
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• W2073648380 title "Counterpoint: Medullary Pacemaker Neurons are Essential for Gasping, but not Eupnea, in Mammals" @default.
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