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Inspiratory on-switch evoked by mesencephalic stimulation: activity of medullary respiratory neurones

Experimental Brain Research volume 56, pages 475–487 (1984)Cite this article

Summary

The activity of medullary inspiratory and expiratory neurones was studied in urethan-chloralose anaesthetized cats during stimulus — evoked inspiratory phase (inspiratory on-switch). All neurones were characterized according to their axonal destination (i.e. bulbospinal neurones or vagal motoneurones) or the absence of such axonal projections (i.e. propriobulbar neurones), and to their location in the dorsal or ventral respiratory nuclei. 1. The inspiratory on-switch effects were elicited during expiration (E phase) by brief tetanic electrical stimulation (50 to 100 ms duration; 0.5 mA; 300 Hz) delivered to the mesencephalic periaqueductal central gray and the adjacent reticular formation. The evoked inspiratory effects observed on the phrenic nerve discharge consisted of: (i) an immediate response (latency 20 ± 5 ms) of stable duration related to the stimulus (primary response: Prim.R.), (ii) a delayed response (patterned response: Patt.R.) appearing after a latent period (silent phase: Sil.P.) of 100 ms maximal duration. The later the stimulus in the E phase, the longer was the duration of the Patt.R. (300 to 1000 ms). 2. The stimulation evoked an earlier activation of the inspiratory bulbospinal neurones (latency 12 ± 6 ms) than that obtained in the phrenic nerve (Prim.R.). Hence, the Prim.R. originated from the bulbospinal pathway and not from a pathway directly impinging on the motoneurones. Conversely during stimulation very few inspiratory propriobulbar neurones were activated and no expiratory neurone discharged. 3. During the phrenic Sil.P., 46% of the inspiratory bulbospinal neurones continued to discharge with a firing rate lower than that during the stimulus train, while most of the inspiratory propriobulbar and expiratory neurones were not active. 4. During the Patt.R. all inspiratory bulbospinal neurones discharged early and were strongly activated whatever the Patt.R. duration whereas the expiratory neurones were not active. Inspiratory propriobulbar neurones were either not recruited or recruited later, and the number of active neurones increased as the duration of the Patt.R. lengthened. 5. Our results suggest that the eliciting of the stimulus-evoked inspiration (Patt.R.) primarily depends on the activation of the inspiratory bulbospinal neurones. These neurones therefore would not only be the output neurones of the medullary respiratory centres, but they would serve other roles such as building up of the excitation in other respiratory neurones, thus acting as a component of the inspiratory ramp generator.

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Abbreviations

Prim.R:

Primary response

Patt.R:

Patterned response

Sil.P:

Silent phase

I phase:

Inspiratory phase

E phase:

Expiratory phase

IBSN:

Inspiratory bulbospinal neurones

IPBN:

Inspiratory propriobulbar neurones

EBSN:

Expiratory bulbospinal neurones

EPBN:

Expiratory propriobulbar neurones

DRN:

Dorsal respiratory nucleus

VRN:

Ventral respiratory nucleus

References

  • Barillot JC, Bianchi AL, Dussardier M, Gauthier P (1980) Study of the validity of the collision test. Application to the bulbospinal respiratory neurons. J Physiol (Paris) 76: 845–858

    Google Scholar 

  • Bassal M, Bianchi AL (1982) Inspiratory onset or termination induced by electrical stimulation of the brain. Respirat Physiol 50: 23–40

    Google Scholar 

  • Bassal M, Bianchi AL, Dussardier M (1981) Effet de la stimulation des structures nerveuses centrales sur l'activité des neurones respiratoires chez le chat. J Physiol (Paris) 77: 779–795

    Google Scholar 

  • Berman AL (1968) The brain stem of the cat. A cytoarchitectonic atlas with stereotaxic coordinates. Madison Univ of Wisconsin Press

  • Bertrand F, Hugelin A (1971) Respiratory synchronizing function of nucleus parabrachialis medialis: pneumotaxic mechanisms. J Neurophysiol 34: 189–207

    Google Scholar 

  • 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 anatomofonctionnelles des neurones respiratoires bulbaires. J. Physiol (Paris) 68: 555–587

    Google Scholar 

  • Bradley GW, von Euler C, Marttila I, Roos R (1975) A model of the central and reflex inhibition of inspiration in the cat. Biol Cybern 19: 105–116

    Google Scholar 

  • Cohen MI (1970) How respiratory rhythm originates: evidence from discharge patterns of brainstem respiratory neurons. In: Porter R (ed), Breathing, Hering-Breuer Centenary Symposium. Churchill, London, pp 125–150

    Google Scholar 

  • Cohen MI (1971) Switching of the respiratory phases and evoked phrenic responses produced by rostral pontine electrical stimulation. J Physiol (London) 217: 133–158

    Google Scholar 

  • Cohen MI (1974) The genesis of respiratory rhythmicity. In: Umbach W, Koepchen HP (eds) Hippokrates, Stuttgart, Central rhythmic and regulation. pp 15–35

  • Cohen MI (1979) Neurogenesis of respiratory rhythm in the mammal. Physiol Rev 59: 1105–1173

    Google Scholar 

  • Cohen MI (1981a) Central determination of respiratory rhythm. Ann Rev Physiol 43: 91–104

    Google Scholar 

  • Cohen MI (1981b) How is respiratory rhythm generated? Fed Proc 40: 2372–2377

    Google Scholar 

  • Cohen MI, Feldman JL (1977) Models of respiratory phaseswitching. Fed Proc 36: 2367–2374

    Google Scholar 

  • Cohen MI, Piercey MF, Gootman PM, Wolotsky P (1974) Synaptic connections between medullary inspiratory neurons and phrenic motoneurons as revealed by cross-correlation. Brain Res 81: 319–324

    Google Scholar 

  • Cohen MI, Piercey MF, Gootman PM, Wolotsky P (1976) Respiratory rhythmicity in the cat. Fed Proc 35: 1967–1974

    Google Scholar 

  • Duffin J, Hockman CH (1972) Limbic forebrain and midbrain modulation and phase-switching of expiratory neurones. Brain Res 39: 235–239

    Google Scholar 

  • Euler C von (1977) The functional organization of the respiratory phase-switching mechanisms. Fed Proc 36: 2375–2380

    Google Scholar 

  • Feldman JL (1981) Interactions between brain stem respiratory neurons. Fed Proc 40: 2384–2388

    Google Scholar 

  • Feldman JL, Speck DF (1983) Interactions among inspiratory neurons in the dorsal and ventral respiratory groups in cat medulla. J Neurophysiol 49: 472–490

    Google Scholar 

  • Feldman JL, Sommer D, Cohen MI (1980) Short time scale correlations between discharges of medullary respiratory neurons. J Neurophysiol 43: 1284–1295

    Google Scholar 

  • Gauthier P, Monteau R, Dussardier M (1983) Inspiratory on-switch evoked by stimulation of mesencephalic structures: a patterned response. Exp Brain Res 51: 261–270

    Google Scholar 

  • Gauthier P, Monteau R, Hilaire G (1984) Inspiratory on-switch evoked by stimulation of the mesencephalon: activity of phrenic and laryngeal motoneurones. Exp Brain Res 55: 197–204

    Google Scholar 

  • Graham K, Duffin J (1982) Cross-correlation of medullary dorsomedial inspiratory neurons in the cat. Exp Neurol 75: 627–643

    Google Scholar 

  • Hilaire G (1979) Contribution à l'étude du contrôle bulbaire de l'activité des motoneurones phréniques chez le chat. Thèse Doctorat ès-Sciences, Marseille

  • Hilaire G, Monteau R (1975) Participation des différents types de neurones bulbaires à l'élaboration de l'activité respiratoire. J Physiol (Paris) 70: 759–777

    Google Scholar 

  • Hilaire G, Monteau R (1976) Connexions entre les neurones inspiratoires bulbaires et les motoneurones phréniques et intercostaux. J Physiol (Paris) 72: 987–1000

    Google Scholar 

  • Hilaire G, Monteau R, Bianchi AL (1984) A cross-correlation study of interactions among respiratory neurons of dorsal, ventral and retrofacial groups in cat medulla. Brain Res 302: 19–31

    Google Scholar 

  • Hockman CH, Duffin J, Ruppert AH, Vachon BR (1974) Phase-switching of respiration induced by central gray and hypocampal stimulation in the cat. J Neurol Trans 35: 327–335

    Google Scholar 

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

    Google Scholar 

  • Jean A, Car A (1979) Inputs to the swallowing medullary neurons from the peripheral afferent fibers and the swallowing cortical area. Brain Res 178: 567–572

    Google Scholar 

  • Madden KP, Remmers JE (1982) Short time scale correlations between spike activity of neighboring respiratory neurons of nucleus tractus solitarius. J Neurophysiol 48: 749–760

    Google Scholar 

  • Merrill EG (1974) Finding a respiratory function for the medullary respiratory neurons. In: Bellairs R, Gray EG (eds), Essays on the nervous system. Clarendon, Oxford, pp 451–486

    Google Scholar 

  • Miller JP, Selverston AI (1979) Rapid killing of single neurons by irradiation of intracellularly injected dye. Science 206: 702–704

    Google Scholar 

  • Mitchell RA (1977) Location and function of medullary respiratory neurons. Am Rev Resp Dis 115, Suppl: 209–216

    Google Scholar 

  • Mitchell RA, Berger AJ (1975) Neural regulation of respiration. Am Rev Respir Dis 111: 206–224

    Google Scholar 

  • Mitchell RA, Herbert DA (1974a) The effect of carbon dioxide on the membrane potential of medullary respiratory neurons. Brain Res 75: 345–349

    Google Scholar 

  • Mitchell RA, Herbert DA (1974b) Synchronized high frequency synaptic potentials in medullary respiratory neurons. Brain Res 75: 350–355

    Google Scholar 

  • Monteau R, Gauthier P (1980) Activité des neurones inspiratoires au cours du déclenchement du programme inspiratoire bulbaire. J Physiol (Paris) 76: 57 A

  • Monteau R, Hilaire G (1977) Recyclage de l'inspiration et polypnée obtenus par stimulation électrique de l'hypothalamus. J Physiol (Paris) 73: 1057–1079

    Google Scholar 

  • Monteau R, Hilaire G (1978) Etude comparée de l'activite' des neurones respiratoires bulbaires lors de polypnée déclenchée par réchauffement ou par stimulation électrique de l'hypothalamus. J Physiol (Paris) 74: 45–55

    Google Scholar 

  • Monteau R, Gauthier P, Hilaire G (1982) Complexité fonctionnelle des prémotoneurones inspiratoires. J Physiol (Paris) 78: 60 A

    Google Scholar 

  • Orem J, Lydic R, Norris P (1979) Experimental control of the diaphragm and laryngeal abductor muscle by brain stem arousal systems. Respirat Physiol 38: 203–221

    Google Scholar 

  • Planche D, Bianchi AL (1972) Modification de l'activité des neurones respiratoires bulbaires provoquée par stimulation corticale. J Physiol (Paris) 64: 69–76

    Google Scholar 

  • Remmers JE, Baker JP, Younes MK (1979) Graded inspiratory inhibition: the first stage of inspiratory “off-switching”. In: Euler C Von, Lagercrantz H (eds), Central nervous control mechanisms in breathing.

  • Richter D (1982) Generation and maintenance of the respiratory rhythm. J Exp Biol 100: 93–107

    Google Scholar 

  • Richter DW, Cammerer H, Meesmann M, Röhrig N (1979) Studies on the synaptic interconnection between bulbar respiratory neurones of cats. Pflügers Arch 380: 245–257

    Google Scholar 

  • Salmoiraghi GC, Burns BD (1960) Localization and patterns of discharge of respiratory neurones in brain-stem of cat. J Neurophysiol 23: 2–13

    Google Scholar 

  • Sears TA, Berger AJ, Phillipson EA (1982) Reciprocal tonic activation of inspiratory and expiratory motoneurones by chemical drive. Nature 299: 728–730

    Google Scholar 

  • Sessle BJ, Greenwood LF, Lund JP, Lucier GE (1978) Effects of upper respiratory tract stimuli on respiration and single respiratory neurons in the adult cat. Exp Neurol 61: 245–259

    Google Scholar 

  • Villard MF, Vibert JF, Caille D, Hugelin A (1981) Effet de la stimulation du noyau de Kölliker-Fuse sur 1-activité de neurones bulbaires à mdoulation respiratoire: recherche de neurones impliqués dans “l'inspiratory off-switch”. J Physiol (Paris) 77: 60 A

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Affiliations

  1. Departement de Physiologie et Neurophysiologie, Faculté des Sciences et Techniques St. Jérôme, Rue Henri Poincaré, F-13397, Marseille Cedex 13, France

    P. Gauthier & R. Monteau

Authors
  1. P. Gauthier
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  2. R. Monteau
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Supported by CNRS (LA 205 and ATP no 4188) and Fondation pour Ia recherche médicale

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Gauthier, P., Monteau, R. Inspiratory on-switch evoked by mesencephalic stimulation: activity of medullary respiratory neurones. Exp Brain Res 56, 475–487 (1984). https://doi.org/10.1007/BF00237988

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  • DOI: https://doi.org/10.1007/BF00237988

Key words

  • Inspiratory on-switch
  • Phrenic nerve
  • Medullary respiratory neurones
  • Central gray
  • Reticular formation
  • Stimulation