Skip to main content
Log in

Activity of dorsal respiratory group inspiratory neurons during laryngeal-induced fictive coughing and swallowing in decerebrate cats

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Membrane potential changes and/or discharges from 36 inspiratory neurons were recorded intracellularly in the dorsal respiratory group (DRG; i.e., the ventrolateral subdivision of the nucleus tractus solitarii) in decerebrate, paralyzed, and ventilated cats. Electrical activities were recorded from both somata (n=10) and axons (n=26). Activities during quiet breathing were compared with those observed during fictive coughing and swallowing evoked by repetitive electrical stimulation of afferent fibers of the superior laryngeal nerve (SLN). These nonrespiratory behaviors were evident in paralyzed animals as characteristic discharge patterns of the phrenic, abdominal, and hypoglossal nerves. Twenty-six neurons exhibiting antidromic action potentials in response to electrical stimuli applied to the cervical (C3–5) spinal cord were classified as inspiratory bulbospinal neurons (IBSNs). These neurons were considered as premotoneurons. The remaining 10 inspiratory neurons (INAA) were not antidromically activated by electrical stimuli applied to either cervical spinal cord or ipsilateral cervical vagus. These neurons are thought to be propriobulbar neurons. We recorded the activity of 31 DRG inspiratory neurons (24 IBSNs and 7 I-NAA) during coughing. All but one (a late-recruited IBSN) discharged a burst of action potentials during the coughing-related phrenic nerve activity. Typically, ramp-like membrane depolarization trajectories and discharge frequencies during coughing were similar to those observed during inspiration. We recorded the activity of 33 DRG inspiratory neurons (23 IBSNs and 10 I-NAA) during swallowing. Most (28/33) neurons were briefly activated, i.e., discharged a burst of action potentials during swallowing, but peak discharge frequency decreased compared with that measured during inspiration. The membrane potentials of nine somata exhibited a brief bell-shaped depolarization during swallowing, the amplitude of which was similar to that observed during inspiration. These results suggest that some inspiratory premotoneurons and propriobulbar neurons of the DRG might be involved in nonrespiratory motor activities, even if clearly antagonistic to breathing (e.g., swallowing). We postulate the existence in the medulla oblongata of adult mammals of neurons exhibiting a “functional flexibility”.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bianchi AL (1971) Localisation et étude des neurones respiratoires bulbaires. Mise en jeu antidromique par stimulation spinale ou vagale. J Physiol (Paris) 63:5–40

    Google Scholar 

  • Bianchi AL (1974) Modalités de décharge et propriétés anatamofonctionelles des neurones respiratoires bulbaires. J Physiol (Paris) 68:555–587

    Google Scholar 

  • Bianchi AL, Grélot L (1989) Converse motor output of inspiratory bulbospinal premotoneurons during vomiting. Neurosci Lett 104:298–302

    Google Scholar 

  • Bianchi AL, Grélot L, Iscoe S, Remmers JE (1988) Electrophysiological properties of rostral medullary respiratory neurons in the cat: an intracellular study. J Physiol (Lond) 407:29–310

    Google Scholar 

  • Bianchi AL, Denavit-Saubié M, Champagnat J (1995) Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. Physiol Rev 75:1–46

    Google Scholar 

  • Bolser D (1991) Fictive cough in the cat. J Appl Physiol 71:2325–2331

    Google Scholar 

  • Contreras RJ, Beckstead RM, Norgren R (1982) The central projections of the trigeminal, facial, glossopharyngeal and vagus nerves: an autoradiographic study in the rat. J Auton Nerv Syst 6:303–322

    Google Scholar 

  • Coombs JS, Curtis DR, Eccles JC (1957) The interpretation of spike potentials of motoneurons. J Physiol (Lond) 139:198–231

    Google Scholar 

  • Dick TE, Oku Y, Romaniuk JR, Cherniack NS (1993) Interaction between central pattern generators for breathing and swallowing in the cat. J Physiol (Lond) 465:715–730

    Google Scholar 

  • Doty RW (1951) Influence of stimulus pattern on reflex deglutition. Am J Physiol 76:142–158

    Google Scholar 

  • Doty RW, Bosma JF (1956) An electromyographic analysis of deglutition. J Neurophysiol 19:44–60

    CAS  PubMed  Google Scholar 

  • Ezure K (1990) Synaptic connexions between medullary respiratory neurons and considerations on the genesis of respiratory rhythm. Prog Neurobiol 35:429–450

    Google Scholar 

  • Fontana GA, Pantaleo T, Bongianni F, Cresci F, Viroli L, Sarago G (1992) Changes in respiratory activity induced by mastication in humans. J Appl Physiol 72:779–786

    Google Scholar 

  • Fortin G, Champagnat J (1993) Spontaneous synaptic activities in rat nucleus tractus solitarius neurons in vitro: evidence for reexcitatory processing. Brain Res 630:125–135

    Google Scholar 

  • Gestreau C, Portillo F, Yousfi-Malki M, Puizillout JJ, Grélot L (1994) Brainstem distribution of c-fos immunoreactivity following repetitive coughing in decerebrate cats. Eur J Neurosci [Suppl] 7:95.01

    Google Scholar 

  • Grélot L (1990) Reconfiguration of the respiratory neuronal network during expulsion and upper airway protective reflexes. In: Neural nets and rhythms in vertebrates and invertebrates, proceedings of an International Symposium. Arcachon, France

    Google Scholar 

  • Grélot L, Milano S (1991) Diaphragmatic and abdominal muscle activities during coughing in the decerebrate cat: a model for fictive coughing. Neuroreport 2:165–168

    Google Scholar 

  • Grélot L, Barillot JC, Bianchi AL (1989) Pharyngeal motoneurons: respiratory-related activity and responses to laryngeal afferents in the decerebrate cat. Exp Brain Res 78:336–344

    Google Scholar 

  • Grélot L, Milano S, Portillo F, Miller AD, Bianchi AL (1992) Membrane potential changes of phrenic motoneurons during fictive vomiting, coughing and swallowing in the decerebrate cat. J Neurophysiol 68:2110–2119

    Google Scholar 

  • Grélot L, Milano S, Portillo F, Miller AD (1993) Respiratory interneurons of the lower cervical (C4–C5) spinal cord: membrane potential changes during coughing, vomiting and swal lowing in the decerebrate cat. Pflugers Arch 425:313–320

    Google Scholar 

  • Hooper SL, Moulins M (1989) Switching of a neuron from one network to another by sensory-induced changes in membrane properties. Science 244:1587–1589

    Google Scholar 

  • Issa FG, Porostocky S (1994) Effect of continuous swallowing on respiration. Resp Physiol 95:181–193

    Google Scholar 

  • Jakus J, Tomori Z, Stransky A (1985) Activity of bulbar respiratory neurons during cough and other respiratory tract reflexes in cats. Physiol Bohemoslov 34:127–136

    Google Scholar 

  • Jean A (1972) Localisation et activité des neurones déglutiteurs bulbaires. J Physiol (Paris) 64:227–268

    Google Scholar 

  • Jean A, Kessler JP, Tell F (1994) Nucleus tractus solitarii and deglutition: monoamines, excitatory amino acids and cellular properties. In: Barraco IRA (ed) Nucleus of the solitary tract. CRC, Boca Raton, Fla, pp 361–376

    Google Scholar 

  • Jiang C, Lipski J (1992) Synaptic inputs to medullary respiratory neurons from superior laryngeal afferents in the cat. Brain Res 584:197–206

    Google Scholar 

  • Jodkowski JS, Berger AJ (1988) Influences from laryngeal afferents on expiratory bulbospinal neurons and motoneurons. J Appl Physiol 64:1337–1345

    Google Scholar 

  • Kase Y, Wakita Y, Kito G, Miyama T, Yuizono T, Kataoka M (1970) Centrally-induced coughs in the cat. Life Sci 9:49–59

    Google Scholar 

  • Kessler JP, Jean A (1985) Identification of the medullary swallowing regions in the rat. Exp Brain Res 57:256–263

    Google Scholar 

  • Kessler JP, Jean A (1991) Evidence that activation of N-methyl-daspartate (NMDA) and non-NMDA receptors within the nucleus tractus solitarii triggers swallowing. Eur J Pharmacol 201:59–67

    Google Scholar 

  • Koga T, Fukuda H (1992) Neurons in the nucleus of the solitary tract mediating inputs from emetic vagal afferents and the area postrema to the pattern generator for the emetic act in dogs. Neurosci Res 14:166–179

    Google Scholar 

  • McFarland DH, Lund JP (1993) An investigation of the coupling between respiration, mastication, and swallowing in the awake rabbit. J Neurophysiol 69:95–108

    Google Scholar 

  • Meyrand P, Simmers J, Moulins M (1991) Construction of a pattern-generating circuit with neurons of different networks. Nature 351:60–63

    Article  CAS  PubMed  Google Scholar 

  • Milano S, Grélot L, Bianchi AL, Iscoe S (1992) Discharge patterns of phrenic motoneurons during fictive coughing and vomiting in decerebrate cat. J Appl Physiol 73:1626–1632

    Google Scholar 

  • Mori M, Sakai Y (1972) Re-examination of centrally-induced cough in cats using a micro-stimulation technique. Jpn J Pharmacol 22:635–643

    Google Scholar 

  • Oku Y, Tanaka I, Ezure K (1994) Activity of bulbar respiratory neurones during fictive coughing and swallowing in the decerebrate cat. J Physiol (Lond) 480(2):309–324

    Google Scholar 

  • Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16:265–297

    Google Scholar 

  • Sasaki K, Otake K, Mannen H, Ezure K, Manabe M (1989) Morphology of augmenting inspiratory neurons of the ventral respiratory group in the cat. J Comp Neurol 282:157–168

    Google Scholar 

  • Shannon R, Morris KE, Lindsey BG (1992) Medullary ventral respiratory group (VRG) neurons responses during fictive coughing. Soc Neurosci Abstr 58.6

    Google Scholar 

  • Sumi T (1963) The activity of brain-stem respiratory neurons and spinal respiratory motoneurons during swallowing. J Neurophysiol 26:466–477

    Google Scholar 

  • Suzuki H, Kondo T, Yamabayashi H, Kobayashi I, Ohta Y (1991) Influence of central respiratory activity on the cough response in anesthetized dogs. Jpn J Physiol 41:879–891

    Google Scholar 

  • Tell F, Jean A (1991) Activation of N-methyl-d-aspartate receptors induces endogenous rhythmic bursting activities in nucleus tractus solitarii neurons: an intracellular study on adult rat brainstem slices. Eur J Neurosci 3:1353–1365

    Google Scholar 

  • Tell F, Jean A (1993) Ionic basis for endogenous rhythmic patterns induced by activation of N-methyl-d-aspartate receptors in neurons of the rat nucleus tractus solitarii. J Neurophysiol 70:2379–2390

    Google Scholar 

  • Tomori Z, Widdicombe JG (1969) Muscular, bronchomotor and cardiovascular reflexes elicited by mechanical stimulation of the respiratory tract. J Physiol (Lond) 200:25–49

    Google Scholar 

  • Von Euler C, Hayward JN, Marttila I, Wyman RJ (1973) Respiratory neurons of the ventrolateral nucleus of the solitary tract in the cat: vagal input, spinal connexions and morphological identification. Brain Res 61:23–33

    Google Scholar 

  • Weimann J, Meyrand P, Marder E (1991) Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. J Neurophysiol 65:111–122

    Google Scholar 

  • Wu JY, Cohen LB, Falk CX (1994) Neuronal activity during different behaviors in aplysia: a distributed organization? Science 263:820–823

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gestreau, C., Milano, S., Bianchi, A.L. et al. Activity of dorsal respiratory group inspiratory neurons during laryngeal-induced fictive coughing and swallowing in decerebrate cats. Exp Brain Res 108, 247–256 (1996). https://doi.org/10.1007/BF00228098

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00228098

Key words

Navigation