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Neural Control of Breathing

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Neural Control of Breathing Available online http://respiratory-research.com/content/2/S1 Meeting abstracts Neural control of breathing An Official Satellite of the International Congress of Physiological Sciences (IUPS) 2001, commentary Rotorua, New Zealand, 1–4 September 2001 Received: 2 August 2001 Respir Res 2001, 2 (suppl 1):S1–S37 © 2001 BioMed Central Ltd Published: 17 August 2001 (Print ISSN 1465-9921; Online ISSN 1465-993X) review ORAL PRESENTATIONS — SESSION 1 pontine and/or afferent respiratory control in Krox-20, Hoxa1 and Ontogeny and phylogeny of respiratory control kreisler mutants. Neonatal respiratory phenotypes are also induced in mice by treatment with low doses of retinoic acid that slightly 1.1 change the early embryonic development of the Pons. Altogether, these experiments indicate that segmentation-related specifica- Early development of respiratory rhythm tions of the hindbrain rhythmic neuronal network influences the res- generation in mice and chicks piratory patterns after birth. Therefore, early developmental J Champagnat, G Fortin, S Jungbluth, V Abadie, F Chatonnet, processes have to be taken into account to understand normal and E Dominquez-del-Toro, L Guimarães pathological diversity of the breathing behaviour in vertebrates. UPR 2216 (Neurobiologie Génétique et Intégrative), IFR 2118 (Institut Acknowledgement: Supported by HFSP RG101/97, ACI (BDPI) reports de Neurobiologie Alfred Fessard), CNRS, 91198, Gif-sur-Yvette, France 2000, CEE BIO4CT, ICCTI PRAXIS XXI (BD/11299/97). Breathing in mammals starts in the foetus and acquires a vital importance at birth. The ability to produce rhythmic motor behav- 1.2 iours linked to respiratory function is a property of the brainstem reticular formation, which has been remarkably conserved during Development of gill and lung breathing in amphibia the evolution of vertebrates. Therefore, to understand the biological MJ Gdovin, VV Jackson, JC Leiter basis of the breathing behavior, we are investigating conservative Division of Life Sciences, University of Texas at San Antonio, TX, USA developmental mechanisms orchestrating the organogenesis of the brainstem. In vertebrates, the hindbrain is one of the vesicles that In the 25 morphological stages of larval bullfrog development there appears at the anterior end of the neural tube of the embryo. exists a gradual transition from gill to lung ventilation associated Further morphogenetic subdivision ensues whereby the hindbrain with a developmental decrease in the contribution of the skin in primary research neuroepithelium becomes partitioned into an iterated series of gas exchange. Bath application of GABA and/or glycine inhibited compartments called rhombomeres. The segmentation process is gill but not lung burst activities of cranial nerve (CN) VII in the believed to determine neuronal fates by encoding positional infor- premetamorphic (stages 16–19) in vitro tadpole brainstem prepa- mation along the rostro-caudal axis. Before and at the onset of seg- ration [1]. It was proposed that the neural basis of gill rhythmogen- mentation, genes encoding transcription factors such as Hox, esis involved network inhibition, whereas lung rhythmicity was Krox-20, kreisler, are expressed in domains corresponding to the pacemaker driven [1]. Bath application of a bicuculline/strychnine limits of future rhombomeres. Inactivation of these genes specifi- solution abolished gill and enhanced lung bursting in stages cally disturbs the rhombomeric pattern of the hindbrain. The pre- 16–19 in vitro [1]. Bath application of the GABAB receptor antago- sentation will address the problem of whether this primordial nist 2-hydroxy-saclofen disinhibited the lung central pattern genera- rhombomeric organisation influences later function of respiratory tor (CPG) resulting in precocious lung bursting patterns as early as control networks in chicks and mice. developmental stage 6 [2]. Experiments were performed in embryos and after birth in trans- We recorded efferent activity from CN VII and spinal nerve (SN) II in genic mice. They show that, although expression of developmental the in vitro tadpole brainstem preparation in three successive devel- meeting abstracts genes and hindbrain segmentation are transient events of early opmental groups (3–9; 10–15; 16–19) before and after bath appli- embryonic development, they are important for the process of res- cation of a 10 µM bicuculline and 5 µM strychnine solution. We also piratory rhythm generation by brainstem neuronal networks. We exposed the brainstem to bath pH 7.4, 7.8, and 8.2 before and after have found in chick that at the end of the period of segmentation, bath application of bicuculline/strychnine. Bicuculline/strychnine the hindbrain contains neuronal rhythm generators that conform to produced lung ventilatory bursts in all developmental stages tested, the rhombomeric anatomical pattern. We have also identified a indicating the presence of the lung CPG as well as excitatory minimal rhombomeric motif allowing the post-segmental maturation synapses to respiratory motor neurons as early as stage 3. of a specific (GABAergic) rhythm-promoting circuit. Furthermore, We also designed an experiment to examine the importance of in vivo and in vitro analysis of neurons in transgenic mice revealed lung ventilation on the developmental shift from gill to lung burst- postnatal respiratory phenotypes associated with defects of central ing. Two groups of tadpoles were hatched from eggs. Control tad- S1 Respiratory Research Vol 2 Suppl 1 Neural control of breathing poles had free access to the air-water interface throughout devel- detected amongst subpopulations of PMNs between ages E16 opment, whereas “barrier” tadpoles were denied access to the air- and P0. 5) There are marked changes in diaphragm muscle con- water interface via the placement of Plexiglas 2.5 cm below the tractile properties that develop in concert with PMN repetitive firing surface of the water. CN VII and SN II efferent activities were properties so that the full-range of diaphragm force recruitment can recorded in vitro at bath pH 7.4, 7.8, and 8.2 before and after bath be utilized at each age and potential problems of diaphragm application of 10 µM bicuculline and 5 µM strychnine. Postmeta- fatigue are minimized. morphic barrier tadpoles exhibited different motor patterns than Data presented will be derived from the following references: stage-matched controls. Tadpoles reared in the barrier condition to 1. Martin-Caraballo M, Greer JJ: Electrophysiological properties of stages 20–25 possessed fictive gill and lung ventilatory activities rat phrenic motoneurons during the perinatal development. J of premetamorphic tadpoles. All barrier tadpole preparations exhib- Neurophysiol 1999, 81:1365–1378 ited robust, spontaneous lung burst activity following bath applica- 2. Greer JJ, Allan DW, Martin-Caraballo M, Lemke RP: Invited tion of bicuculline/strychnine. Review: An overview of phrenic nerve and diaphragm muscle We propose that developmentally dependent GABA- and glyciner- development in the perinatal rat. J Appl Physiol 1999, gic mechanisms lead to disinhibition of the lung CPG such that 86:779–786 early in development gill motor patterns are the dominant respiratory 3. Martin-Caraballo M, Campagnaro PA, Gao Y, Greer JJ: Contrac- rhythm, whereas in late development the lung CPG is the dominant tile properties of the rat diaphragm during the perinatal respiratory rhythm. Denying the tadpole the ability to “practice” lung period. J Appl Physiol 2000, 88:573–580 breathing during metamorphosis produces a morphologically 4. Martin-Caraballo M, Greer JJ: Development of potassium con- correct postmetamorphic tadpole with an immature, or premetamor- ductances in perinatal rat phrenic motoneurons. J Neurophys- phic respiratory rhythm. We propose that prevention of lung inflation iol 2000, 83:3497–3508 in barrier tadpoles leads to premetamorphic levels of GABA- and 5. Martin-Caraballo M, Greer JJ: Voltage-sensitive calcium cur- glycinergic inhibition, and that this inhibition may be altered by pul- rents and their role in regulating phrenic motoneuron electri- monary stretch receptor feedback in control tadpoles. cal excitability during the perinatal period. J Neurobiol 2001, 46:231–248 References 1. Galante RJ, Kubin L, Fishman AP, Pack AI: Role of chloride- Acknowledgements: Funded by CIHR, AHFMR and Alberta Lung mediated inhibition in respiratory rhythmogenesis in an in Association. vitro brainstem of tadpole, Rana catesbeiana. J Physiol 1996, 492:545–558 1.4 2. Straus C, Wilson RJA, Remmers JE: Developmental disinhibi- tion: turning off inhibition turns on breathing in vertebrates. J Central neuromodulation and adaptations during Neurobiol 2000, 45:75–83 respiratory development IR Moss, A Laferrière, J-K Liu Acknowledgement: Approved by the University of Texas at San Developmental Respiratory Laboratory, McGill University Health Antonio Animal Care Committee. Supported by the NIH NINDS Centre Research Institute, Montreal Children’s Hospital, Montreal, Specialized Neuroscience Research Program. Quebec, Canada 1.3 Consecutive daily hypoxia in developing swine results in a relatively lower hyperventilatory response than does a single exposure to the Phrenic motoneuron and diaphragm development same hypoxic protocol [1]. We have hypothesized that this relative during the perinatal period hypoventilation is associated with a decreased excitatory versus JJ Greer, M Martin-Caraballo inhibitory neuromodulatory influence on central integrative path- ways of breathing
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