Top

Published in:

Open Access 01-01-2019 | Original Article

Structural and functional identification of two distinct inspiratory neuronal populations at the level of the phrenic nucleus in the rat cervical spinal cord

Authors: Yoshio Shinozaki, Shigefumi Yokota, Fumikazu Miwakeichi, Mieczyslaw Pokorski, Ryoma Aoyama, Kentaro Fukuda, Hideaki Yoshida, Yoshiaki Toyama, Masaya Nakamura, Yasumasa Okada

Published in: Brain Structure and Function | Issue 1/2019

Abstract

The diaphragm is driven by phrenic motoneurons that are located in the cervical spinal cord. Although the anatomical location of the phrenic nucleus and the function of phrenic motoneurons at a single cellular level have been extensively analyzed, the spatiotemporal dynamics of phrenic motoneuron group activity have not been fully elucidated. In the present study, we analyzed the functional and structural characteristics of respiratory neuron population in the cervical spinal cord at the level of the phrenic nucleus by voltage imaging, together with histological analysis of neuronal and astrocytic distribution in the cervical spinal cord. We found spatially distinct two cellular populations that exhibited synchronized inspiratory activity on the transversely cut plane at C4–C5 levels and on the ventral surface of the mid cervical spinal cord in the isolated brainstem–spinal cord preparation of the neonatal rat. Inspiratory activity of one group emerged in the central portion of the ventral horn that corresponded to the central motor column, and the other appeared in the medial portion of the ventral horn that corresponded to the medial motor column. We identified by retrogradely labeling study that the anatomical distributions of phrenic and scalene motoneurons coincided with optically detected central and medial motor regions, respectively. Furthermore, we anatomically demonstrated closely located features of putative motoneurons, interneurons and astrocytes in these regions. Collectively, we report that phrenic and scalene motoneuron populations show synchronized inspiratory activities with distinct anatomical locations in the mid cervical spinal cord.

Allan DW, Greer JJ (1997) Development of phrenic motoneuron morphology in the fetal rat. J Comp Neurol 382:469–479PubMedCrossRef

Anderson WJ, Bellinger DL, Lorton D (1988) Morphology of dendrite bundles in the cervical spinal cord of the rat: a light microscopic study. Exp Neurol 100:121–138PubMedCrossRef

Aoyama R, Okada Y, Yokota S, Yasui Y, Fukuda K, Shinozaki Y, Yoshida H, Nakamura M, Chiba K, Yasui Y, Kato F, Toyama Y (2011) Spatiotemporal and anatomical analyses of P2X receptor-mediated neuronal and glial processing of sensory signals in the rat dorsal horn. Pain 152:2085–2097. https://doi.org/10.1016/j.pain.2011.05.014 PubMedCrossRef

Bader A, Klein B, Breer H, Strotmann J (2012) Connectivity from OR37 expressing olfactory sensory neurons to distinct cell types in the hypothalamus. Front Neural Circuits 6:84. https://doi.org/10.3389/fncir.2012.00084 PubMedPubMedCentralCrossRef

Barber RP, Phelps PE, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE (1984) The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: an immunocytochemical study. J Comp Neurol 229(3):329–346PubMedCrossRef

Bellingham MC, Lipski J (1990) Respiratory interneurons in the C5 segment of the spinal cord of the cat. Brain Res 533:141–146PubMedCrossRef

Berger AJ (1979) Phrenic motoneurons in the cat: subpopulations and nature of respiratory drive potentials. J Neurophysiol 42:76–90PubMedCrossRef

Brichta AM, Callister RJ, Peterson EH (1987) Quantitative analysis of cervical musculature in rats: histochemical composition and motor pool organization. I. Muscles of the spinal accessory complex. J Comp Neurol 255:351–368PubMedCrossRef

Butt SJ, Harris-Warrick RM, Kiehn O (2002) Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator. J Neurosci 22:9961–9971PubMedPubMedCentralCrossRef

Cameron WE, Nunez-Abades PA (2000) Physiological changes accompanying anatomical remodeling of mammalian motoneurons during postnatal development. Brain Res Bull 53:523–527PubMedCrossRef

Cameron WE, Averill DB, Berger AJ (1983) Morphology of cat phrenic motoneurons as revealed by intracellular injection of horseradish peroxidase. J Comp Neurol 219:70–80PubMedCrossRef

Cameron WE, Brozanski BS, Guthrie RD (1990) Postnatal development of phrenic motoneurons in the cat. Brain Res Dev Brain Res 51:142–145PubMedCrossRef

Cameron WE, He F, Kalipatnapu P, Jodkowski JS, Guthrie RD (1991) Morphometric analysis of phrenic motoneurons in the cat during postnatal development. J Comp Neurol 314:763–776PubMedCrossRef

Campbell EJ (1955) The role of the scalene and sternomastoid muscles in breathing in normal subjects; an electromyographic study. J Anat 89:378–386PubMedPubMedCentral

Christensen RK, Petersen AV, Perrier JF (2013) How do glial cells contribute to motor control? Curr Pharm Des 19(24):4385–4399PubMedCrossRef

Critchlow V, von Euler C (1963) Intercostal muscle spindle activity and its γ-motor control. J Physiol 168:820–847PubMedPubMedCentralCrossRef

D’Angelo E, Bellemare F (1990) Electrical and mechanical output of the inspiratory muscles in anesthetized dogs. Respir Physiol 79(2):177–193PubMedCrossRef

D’Angelo E, Garzaniti N, Bellemare F (1988) Inspiratory muscle activity during unloaded and obstructed rebreathing in dogs. J Appl Physiol (1985) 64:90–101CrossRef

De Troyer A, Estenne M (1984) Coordination between rib cage muscles and diaphragm during quiet breathing in humans. J Appl Physiol Respir Environ Exerc Physiol 57(3):899–906. https://doi.org/10.1152/jappl.1984.57.3.899 PubMedCrossRef

Elliott HC (1942) Studies on the motor cells of the spinal cord. I. Distribution in the normal human cord. Am J Anat 70:95–117CrossRef

Fournier M, Lewis MI (1996) Functional role and structure of the scalene: an accessory inspiratory muscle in hamster. J Appl Physiol (1985) 81:2436–2444CrossRef

Fukuda K, Okada Y, Yoshida H, Aoyama R, Nakamura M, Chiba K, Toyama Y (2006) Ischemia-induced disturbance of neural network function in the rat spinal cord analyzed by voltage-imaging. Neuroscience 140(4):1453–1465. https://doi.org/10.1016/j.neuroscience.2006.03.034 PubMedCrossRef

Fukushi I, Takeda K, Yokota S, Hasebe Y, Sato Y, Pokorski M, Horiuchi J, Okada Y (2016) Effects of arundic acid, an astrocytic modulator, on the cerebral and respiratory functions in severe hypoxia. Respir Physiol Neurobiol 226:24–29. https://doi.org/10.1016/j.resp.2015.11.011 PubMedCrossRef

Furicchia JV, Goshgarian HG (1987) Dendritic organization of phrenic motoneurons in the adult rat. Exp Neurol 96:621–634PubMedCrossRef

Gill PK, Kuno M (1963a) Excitatory and inhibitory actions on phrenic motoneurones. J Physiol 168:274–289PubMedPubMedCentralCrossRef

Gill PK, Kuno M (1963b) Properties of phrenic motoneurones. J Physiol 168:258–273PubMedPubMedCentralCrossRef

Gittins R, Harrison PJ (2004) Neuronal density, size and shape in the human anterior cingulate cortex: a comparison of Nissl and NeuN staining. Brain Res Bull 63(2):155–160. https://doi.org/10.1016/j.brainresbull.2004.02.005 PubMedCrossRef

Gordon DC, Richmond FJ (1990) Topography in the phrenic motoneuron nucleus demonstrated by retrograde multiple-labelling techniques. J Comp Neurol 292:424–434PubMedCrossRef

Goshgarian HG, Rafols JA (1981) The phrenic nucleus of the albino rat: a correlative HRP and Golgi study. J Comp Neurol 201:441–456PubMedCrossRef

Goshgarian HG, Rafols JA (1984) The ultrastructure and synaptic architecture of phrenic motor neurons in the spinal cord of the adult rat. J Neurocytol 13:85–109PubMedCrossRef

Goshgarian HG, Roubal PJ (1986) Origin and distribution of phrenic primary afferent nerve fibers in the spinal cord of the adult rat. Exp Neurol 92:624–638PubMedCrossRef

Goshgarian HG, Yu XJ (1990) Chronic hypoxia causes morphological alterations in astroglia in the phrenic nucleus of young adult rats. Exp Neurol 107:170–177PubMedCrossRef

Goshgarian HG, Yu XJ, Rafols JA (1989) Neuronal and glial changes in the rat phrenic nucleus occurring within hours after spinal cord injury. J Comp Neurol 284:519–533PubMedCrossRef

Goshgarian HG, Ellenberger HH, Feldman JL (1991) Decussation of bulbospinal respiratory axons at the level of the phrenic nuclei in adult rats: a possible substrate for the crossed phrenic phenomenon. Exp Neurol 111:135–139PubMedCrossRef

Henneberger C, Papouin T, Oliet SH, Rusakov DA (2010) Long-term potentiation depends on release of d-serine from astrocytes. Nature 463(7278):232–236. https://doi.org/10.1038/nature08673 PubMedPubMedCentralCrossRef

Hollinshead WH, Keswani NH (1956) Localization of the phrenic nucleus in the spinal cord of man. Anat Rec 125:683–699PubMedCrossRef

Huang Y, Goshgarian HG (2009) Identification of the neural pathway underlying spontaneous crossed phrenic activity in neonatal rats. Neuroscience 163(4):1109–1118. https://doi.org/10.1016/j.neuroscience.2009.07.011 PubMedPubMedCentralCrossRef

Iizuka M, Onimaru H, Izumizaki M (2016) Distribution of respiration-related neuronal activity in the thoracic spinal cord of the neonatal rat: an optical imaging study. Neuroscience 315:217–227. https://doi.org/10.1016/j.neuroscience.2015.12.015 PubMedCrossRef

Johnson SM, Getting PA (1988) Phrenic motor nucleus of the guinea pig: dendrites are bundled without clustering of cell somas. Exp Neurol 101:208–220PubMedCrossRef

Kawai A, Ballantyne D, Mückenhoff K, Scheid P (1996) Chemosensitive medullary neurones in the brainstem–spinal cord preparation of the neonatal rat. J Physiol 492:277–292PubMedPubMedCentralCrossRef

Kawai A, Onimaru H, Homma I (2006) Mechanisms of CO₂/H⁺ chemoreception by respiratory rhythm generator neurons in the medulla from newborn rats in vitro. J Physiol 572:525–537. https://doi.org/10.1113/jphysiol.2005.102533 PubMedPubMedCentralCrossRef

Keswani NH, Hollinshead WH (1955) The phrenic nucleus. III. Organization of the phrenic nucleus in the spinal cord of the cat and man. Proc Staff Meet Mayo Clin 30:566–577PubMed

Kondo T, Funayama M, Tsukita K, Hotta A, Yasuda A, Nori S, Kaneko S, Nakamura M, Takahashi R, Okano H, Yamanaka S, Inoue H (2014) Focal transplantation of human iPSC-derived glial-rich neural progenitors improves lifespan of ALS mice. Stem Cell Rep 3(2):242–249. https://doi.org/10.1016/j.stemcr.2014.05.017 CrossRef

Korzhevskii DE, Otellin VA (2005) Immunocytochemical detection of astrocytes in brain slices in combination with Nissl staining. Neurosci Behav Physiol 35(6):639–641PubMedCrossRef

Koshiya N, Oku Y, Yokota S, Oyamada Y, Yasui Y, Okada Y (2014) Anatomical and functional pathways of rhythmogenic inspiratory premotor information flow originating in the pre-Bötzinger complex in the rat medulla. Neuroscience 268:194–211. https://doi.org/10.1016/j.neuroscience.2014.03.002 PubMedCrossRef

Kuzuhara S, Chou SM (1980) Localization of the phrenic nucleus in the rat: a HRP study. Neurosci Lett 16:119–124PubMedCrossRef

Lane MA (2011) Spinal respiratory motoneurons and interneurons. Respir Physiol Neurobiol 179(1):3–13. https://doi.org/10.1016/j.resp.2011.07.004 PubMedCrossRef

Lane MA, White TE, Coutts MA, Jones AL, Sandhu MS, Bloom DC, Bolser DC, Yates BJ, Fuller DD, Reier PJ (2008) Cervical prephrenic interneurons in the normal and lesioned spinal cord of the adult rat. J Comp Neurol 511(5):692–709. https://doi.org/10.1002/cne.21864 PubMedPubMedCentralCrossRef

Lee KZ, Fuller DD (2011) Neural control of phrenic motoneuron discharge. Respir Physiol Neurobiol 179(1):71–79. https://doi.org/10.1016/j.resp.2011.02.014 PubMedPubMedCentralCrossRef

Li K, Javed E, Scura D, Hala TJ, Seetharam S, Falnikar A, Richard JP, Chorath A, Maragakis NJ, Wright MC, Lepore AC (2015) Human iPS cell-derived astrocyte transplants preserve respiratory function after spinal cord injury. Exp Neurol 271:479–492. https://doi.org/10.1016/j.expneurol.2015.07.020 PubMedPubMedCentralCrossRef

Lindsay AD, Greer JJ, Feldman JL (1991) Phrenic motoneuron morphology in the neonatal rat. J Comp Neurol 308:169–179PubMedCrossRef

Liu G, Feldman JL (1992) Quantal synaptic transmission in phrenic motor nucleus. J Neurophysiol 68:1468–1471PubMedCrossRef

Martin-Caraballo M, Greer JJ (1999) Electrophysiological properties of rat phrenic motoneurons during perinatal development. J Neurophysiol 81(3):1365–1378. https://doi.org/10.1152/jn.1999.81.3.1365 PubMedCrossRef

Martin-Caraballo M, Greer JJ (2000) Development of potassium conductances in perinatal rat phrenic motoneurons. J Neurophysiol 83(6):3497–3508. https://doi.org/10.1152/jn.2000.83.6.3497 PubMedCrossRef

Martin-Caraballo M, Greer JJ (2001) Voltage-sensitive calcium currents and their role in regulating phrenic motoneuron electrical excitability during the perinatal period. J Neurobiol 46(4):231–248PubMedCrossRef

Matsui T, Akamatsu W, Nakamura M, Okano H (2014) Regeneration of the damaged central nervous system through reprogramming technology: basic concepts and potential application for cell replacement therapy. Exp Neurol 260:12–18. https://doi.org/10.1016/j.expneurol.2012.09.016 PubMedCrossRef

Mitchell GA, Warwick R (1956) The phrenic nucleus of the macaque. J Comp Neurol 105:553–585PubMedCrossRef

Molander C, Xu Q, Rivero-Melian C, Grant G (1989) Cytoarchitectonic organization of the spinal cord in the rat: II. The cervical and upper thoracic cord. J Comp Neurol 289:375–385PubMedCrossRef

Monteau R, Hilaire G (1991) Spinal respiratory motoneurons. Prog Neurobiol 37:83–144PubMedCrossRef

Nakamura M, Okano H (2013) Cell transplantation therapies for spinal cord injury focusing on induced pluripotent stem cells. Cell Res 23(1):70–80. https://doi.org/10.1038/cr.2012.171 PubMedCrossRef

Okada Y, Mückenhoff K, Scheid P (1993) Hypercapnia and medullary neurons in the isolated brain stem-spinal cord of the rat. Respir Physiol 93:327–336PubMedCrossRef

Okada Y, Kuwana S, Kawai A, Mückenhoff K, Scheid P (2005) Significance of extracellular potassium in central respiratory control studied in the isolated brainstem-spinal cord preparation of the neonatal rat. Respir Physiol Neurobiol 146(1):21–32. https://doi.org/10.1016/j.resp.2004.10.009 PubMedCrossRef

Okada Y, Masumiya H, Tamura Y, Oku Y (2007) Respiratory and metabolic acidosis differentially affect the respiratory neuronal network in the ventral medulla of neonatal rats. Eur J Neurosci 26(10):2834–2843. https://doi.org/10.1111/j.1460-9568.2007.05891.x PubMedCrossRef

Okada Y, Yokota S, Shinozaki Y, Miwakeichi F, Oku Y, Yasui Y (2010) Anatomical changes of phrenic motoneurons during development. Adv Exp Med Biol 669:33–36. https://doi.org/10.1007/978-1-4419-5692-7_7 PubMedCrossRef

Okada Y, Sasaki T, Oku Y, Takahashi N, Seki M, Ujita S, Tanaka KF, Matsuki N, Ikegaya Y (2012) Preinspiratory calcium rise in putative pre-Bötzinger complex astrocytes. J Physiol 590(19):4933–4944. https://doi.org/10.1113/jphysiol.2012.231464 PubMedPubMedCentralCrossRef

Oku Y, Masumiya H, Okada Y (2007) Postnatal developmental changes in activation profiles of the respiratory neuronal network in the rat ventral medulla. J Physiol 585:175–186. https://doi.org/10.1113/jphysiol.2007.138180 PubMedPubMedCentralCrossRef

Oku Y, Okabe A, Hayakawa T, Okada Y (2008) Respiratory neuron group in the high cervical spinal cord discovered by optical imaging. Neuroreport 19(17):1739–1743. https://doi.org/10.1097/WNR.0b013e328318edb5 PubMedCrossRef

Onimaru H, Homma I (2003) A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23(4):1478–1486PubMedPubMedCentralCrossRef

Ono K, Tsumori T, Kishi T, Yokota S, Yasui Y (1998) Developmental appearance of oligodendrocytes in the embryonic chick retina. J Comp Neurol 398(3):309–322PubMedCrossRef

Paxinos G, Törk I, Tecott LH, Valentino KL (1991) Atlas of the developing rat brain. Academic Press, San Diego

Poole DC, Sexton WL, Farkas GA, Powers SK, Reid MB (1997) Diaphragm structure and function in health and disease. Med Sci Sports Exerc 29:738–754PubMedCrossRef

Prakash YS, Mantilla CB, Zhan WZ, Smithson KG, Sieck GC (2000) Phrenic motoneuron morphology during rapid diaphragm muscle growth. J Appl Physiol (1985) 89(2):563–572. https://doi.org/10.1152/jappl.2000.89.2.563 CrossRef

Qiu K, Lane MA, Lee KZ, Reier PJ, Fuller DD (2010) The phrenic motor nucleus in the adult mouse. Exp Neurol 226(1):254–258. https://doi.org/10.1016/j.expneurol.2010.08.026 PubMedPubMedCentralCrossRef

Rao GS, Saigal RP, Sahu S (1972) The phrenic nerve and the localisation of phrenic nucleus in the spinal cord of the buffalo (Bubalus bubalis). Acta Anat (Basel) 83:468–477CrossRef

Rikard-Bell GC, Bystrzycka EK (1980) Localization of phrenic motor nucleus in the cat and rabbit studied with horseradish peroxidase. Brain Res 194:479–483PubMedCrossRef

Rose D, Larnicol N, Duron B (1984) An HRP study of the cat’s spinal respiratory motoneurones during postnatal development. Exp Brain Res 56:458–467PubMedCrossRef

Routal RV, Pal GP (1999) Location of the phrenic nucleus in the human spinal cord. J Anat 195:617–621PubMedPubMedCentralCrossRef

Saboisky JP, Gorman RB, De Troyer A, Gandevia SC, Butler JE (2007) Differential activation among five human inspiratory motoneuron pools during tidal breathing. J Appl Physiol (1985) 102(2):772–780. https://doi.org/10.1152/japplphysiol.00683.2006 CrossRef

Sakamoto Y (2012) Spatial relationships between the morphologies and innervations of the scalene and anterior vertebral muscles. Ann Anat 194(4):381–388. https://doi.org/10.1016/j.aanat.2011.11.004 PubMedCrossRef

Sant’ambrogio G, Camporesi E (1973) Contribution of various inspiratory muscles to ventilation and the immediate and distant effect of diaphragmatic paralysis. Acta Neurobiol Exp (Wars) 33(1):401–409

Sheikhbahaei S, Turovsky EA, Hosford PS, Hadjihambi A, Theparambil SM, Liu B, Marina N, Teschemacher AG, Kasparov S, Smith JC, Gourine AV (2018) Astrocytes modulate brainstem respiratory rhythm-generating circuits and determine exercise capacity. Nat Commun 9(1):370. https://doi.org/10.1038/s41467-017-02723-6 PubMedPubMedCentralCrossRef

Smith JC, Liu G, Feldman JL (1988) Intracellular recording from phrenic motoneurons receiving respiratory drive in vitro. Neurosci Lett 88:27–32PubMedCrossRef

Song A, Ashwell KW, Tracey DJ (2000) Development of the rat phrenic nucleus and its connections with brainstem respiratory nuclei. Anat Embryol (Berl) 202(2):159–177. https://doi.org/10.1007/s004290000096 CrossRef

St John WM, Bartlett D Jr (1985) Comparison of phrenic motoneuron activity in eupnea and apneusis. Respir Physiol 60(3):347–355PubMedCrossRef

Streeter KA, Sunshine MD, Patel SR, Liddell SS, Denholtz LE, Reier PJ, Fuller DD, Baekey DM (2017) Coupling multielectrode array recordings with silver labeling of recording sites to study cervical spinal network connectivity. J Neurophysiol 117(3):1014–1029. https://doi.org/10.1152/jn.00638.2016 PubMedCrossRef

Takahashi K, Ninomiya T (1985) Observations on the fine structure of the phrenic nucleus in the cervical spinal cord of the cat with special reference to its dendritic bundles. J Anat 140:491–498PubMedPubMedCentral

Takahashi K, Satomi H, Ise H, Yamamoto T (1980) Identification of the phrenic nucleus in the cat as studied by horseradish peroxidase bathing of the transected intrathoracal phrenic nerve. Anat Anz 148(1):49–54PubMed

Tanaka KF, Matsui K, Sasaki T, Sano H, Sugio S, Fan K, Hen R, Nakai J, Yanagawa Y, Hasuwa H, Okabe M, Deisseroth K, Ikenaka K, Yamanaka A (2012) Expanding the repertoire of optogenetically targeted cells with an enhanced gene expression system. Cell Rep 2(2):397–406. https://doi.org/10.1016/j.celrep.2012.06.011 PubMedCrossRef

Torikai H, Hayashi F, Tanaka K, Chiba T, Fukuda Y, Moriya H (1996) Recruitment order and dendritic morphology of rat phrenic motoneurons. J Comp Neurol 366:231–243PubMedCrossRef

Ullah M (1978) Localization of the phrenic nucleus in the spinal cord of the rabbit. J Anat 125:377–386PubMedPubMedCentral

Warren PM, Alilain WJ (2014) The challenges of respiratory motor system recovery following cervical spinal cord injury. Prog Brain Res 212:173–220. https://doi.org/10.1016/B978-0-444-63488-7.00010-0 PubMedCrossRef

Warwick R, Mitchell GAG (1956) The phrenic nucleus of the macaque. J Comp Neurol 105:553–585PubMedCrossRef

Webber CL Jr, Wurster RD, Chung JM (1979) Cat phrenic nucleus architecture as revealed by horseradish peroxidase mapping. Exp Brain Res 35(3):395–406PubMedCrossRef

Windelborn JA, Mitchell GS (2012) Glial activation in the spinal ventral horn caudal to cervical injury. Respir Physiol Neurobiol 180(1):61–68. https://doi.org/10.1016/j.resp.2011.10.011 PubMedCrossRef

Yokota S, Tsumori T, Ono K, Yasui Y (2004) Glutamatergic pathways from the Kölliker-Fuse nucleus to the phrenic nucleus in the rat. Brain Res 995(1):118–130PubMedCrossRef

Yokota S, Oka T, Tsumori T, Nakamura S, Yasui Y (2007) Glutamatergic neurons in the Kölliker-Fuse nucleus project to the rostral ventral respiratory group and phrenic nucleus: a combined retrograde tracing and in situ hybridization study in the rat. Neurosci Res 59(3):341–346. https://doi.org/10.1016/j.neures.2007.08.004 PubMedCrossRef

Yokota S, Tsumori T, Oka T, Nakamura S, Yasui Y (2008) GABAergic neurons in the ventrolateral subnucleus of the nucleus tractus solitarius are in contact with Kölliker-Fuse nucleus neurons projecting to the rostral ventral respiratory group and phrenic nucleus in the rat. Brain Res 1228:113–126. https://doi.org/10.1016/j.brainres.2008.06.089 PubMedCrossRef

Yokota S, Shinozaki Y, Oku Y, Okada Y, Yasui Y (2010) Vesicular glutamate transporter 2-immunoreactive synapses onto phrenic motoneurons in the neonatal rat. Adv Exp Med Biol 669:189–192. https://doi.org/10.1007/978-1-4419-5692-7_38 PubMedCrossRef

Yoshida H, Okada Y, Maruiwa H, Fukuda K, Nakamura M, Chiba K, Toyama Y (2003) Synaptic blockade plays a major role in the neural disturbance of experimental spinal cord compression. J Neurotrauma 20(12):1365–1376. https://doi.org/10.1089/089771503322686157 PubMedCrossRef

Zimmer MB, Goshgarian HG (2005) Spontaneous crossed phrenic activity in the neonatal respiratory network. Exp Neurol 194(2):530–540. https://doi.org/10.1016/j.expneurol.2005.03.013 PubMedCrossRef

Title: Structural and functional identification of two distinct inspiratory neuronal populations at the level of the phrenic nucleus in the rat cervical spinal cord
Authors: Yoshio Shinozaki
Shigefumi Yokota
Fumikazu Miwakeichi
Mieczyslaw Pokorski
Ryoma Aoyama
Kentaro Fukuda
Hideaki Yoshida
Yoshiaki Toyama
Masaya Nakamura
Yasumasa Okada
Publication date: 01-01-2019
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 1/2019
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1757-3

At a glance: The STEP trials

Springer Medicine

Structural and functional identification of two distinct inspiratory neuronal populations at the level of the phrenic nucleus in the rat cervical spinal cord

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2019

Melanin-concentrating hormone neurons promote rapid eye movement sleep independent of glutamate release

Central relaxin-3 receptor (RXFP3) activation impairs social recognition and modulates ERK-phosphorylation in specific GABAergic amygdala neurons

Modulation of olfactory-driven behavior by metabolic signals: role of the piriform cortex

Medium spiny neurons of the anterior dorsomedial striatum mediate reversal learning in a cell-type-dependent manner

Linking structural and effective brain connectivity: structurally informed Parametric Empirical Bayes (si-PEB)

TMS of the occipital face area modulates cross-domain identity priming