Abstract
Using microinjection techniques, we have explored the isolated, complete midline sectioned brainstem of the frog (Rana catesbeiana) to identify regions that influence the endogenous respiratory-related motor activity. Ten-nanoliter injections of lidocaine (1%), GABA (100 mM) and glutamate (10 and 100 mM) into discrete regions of the rostral and the caudal brainstem produced different effects on the phasic neural discharge. In the rostral site lidocaine, GABA and glutamate injections altered neural burst frequency with little or no effect on burst amplitude. In the caudal site, responses to lidocaine and GABA injections consisted primarily of decreases in neural burst amplitude, often, but not always associated with minor decreases in burst frequency. In this same region, the response to glutamate was characterized by a temporary interruption of the rhythmic neural burst activity. The largest responses to substance injection in both regions were obtained at sites ranging between 200 and 500 μm from the ventral surface, in the ventral medullary reticular formation. The results reveal the existence of two areas in the frog brainstem that influence respiratory motor output, one related to the respiratory burst frequency and the other related to the amplitude of the motor output.
Similar content being viewed by others
Abbreviations
- V :
-
trigeminal nerve
- VI :
-
abducens nerve
- VII :
-
facial nerve
- VIII :
-
auditory nerve
- X :
-
vagal nerve
- H :
-
hypoglossal nerve
- VRG :
-
ventral respiratory group
- NTS :
-
nucleus of the solitary tract
References
Aoki M, Mori S, Kawahara K, Watanabe H, Ebata N (1980) Generation of spontaneous respiratory rhythm in high spinal cats. Brain Res 202: 51–63
Bongianni F, Fontana G, Pantaleo T (1988) Effects of electrical and chemical stimulation of the Bötzinger complex on respiratory activity in the cat. Brain Res 445: 254–261
Budzinska K, von Euler C, Kao RR, Panteleo T, Yamamoto Y (1985) Effects of graded cold block in rostral areas of the medulla. Acta Physiol Scand 124: 329–340
Champagnat J, Denavit-Saubié M, Velluti JC (1980) Excitability of bulbar respiratory neurones: a study using microiontophoretic applications of depolarizing agents. Brain Res 191: 359–377
Curtis DR, Phillis JW, Watkins JC (1960) The chemical excitation of spinal neurones by certain acidic amino acids. J Physiol (Lond) 150: 656–682
de Jongh HJ and Gans C (1969) Breathing movements in the bullfrog Rana catesbeiana: a reassessment. J Morphol 127: 259–290
Ezure K (1990) Synaptic connections between medullary respiratory neurons and considerations on the genesis of respiratory rhythm. Prog Neurobiol 35: 429–450
Goodchild AK, Dempney RAL, Bandler R (1982) A method for evoking physiological responses by stimulation of cell bodies, but not axons of passage, within localized regions of the central nervous system. J Neurosci Meth 6: 351–363
Haji A, Remmers JE, Connelly C, Takada R (1990) Effects of glycine and GABA on bulbar respiratory neurons of the cat. J Neurophysiol 63: 955–965
Haji A, Takeda R, Remmers JE (1992) Evidence that glycine and GABA mediate postsynaptic inhibition of bulbar respiratory neurons in the cat. J Appl Physiol 73: 2333–2342
Homma I, Isobe A, Iwase M, Kanamaru A, Sibuya M (1988) Two different types of apnea induced by focal cold block of ventral medulla in rabbits. Neurosci Lett 87: 41–45
Issa F, Remmers JE (1992) Identification of a sub-surface area in the ventral medulla sensitive to local changes in PCO2. J Appl Physiol 72: 439–446
Karczewski WA, Gromysz H (1982) The significance of species differences in respiratory neurophysiology — the split-brainstem preparation. Experientia 38: 826–827
Kirsten EB, Satayavivad J, St. John W, Wang SC (1978) Alteration of medullary respiratory unit discharge by iontophoretic application of putative neurotransmitters. Br J Pharmacol 63: 275–281
Kogo N, Perry SF, Remmers JE (1994) Neural organization of the ventilatory activity of the frog, Rana catesbeiana. I. J Neurobiol 25: 1067–1079
Kulenbeck H (1975) (ed) The central nervous system of vertebrates. Karger, New York
Langendorff O (1887) Die Automatie des Atemzentrums. Arch Anat Physiol 285–295
Lipski J, Bellingham MC, West MJ, Pilowsky P (1988) Limitations of the technique of pressure microinjection of excitatory amino acids for evoking responses from localized regions of the CNS. J Neurosci Meth 26: 169–179
Lumsden T (1923) Observations on the respiratory centers in the cat. J Physiol (Lond) 57: 354–367
McCrimmon DR, Feldman JL, Speck DR (1986) Respiratory motoneuronal activity is altered by injections of picomoles of glutamate into cat brain stem. J Neurosci 6: 2384–2392
McLean HA, Remmers JE (1994) Respiratory motor output of the sectioned medulla of the neonatal rat. Resp Physiol 96: 49–60
McLean HA, Kimura N, Kogo N, Perry SF, Remmers JE (1995) Fictive respiratory rhythm in the isolated brainstem of frogs. J Comp Physiol A 176: 703–713
Morin-Surun MP, Champagnat J, Boudinot E, Denavit-Saubié M (1984) Differentiation of two respiratory areas in the cat medulla using kainic acid. Resp Physiol 58: 323–334
Murakoshi T, Suzue T, Tamai S (1985) A pharmacological study on respiratory rhythm in the isolated brainstem-spinal cord preparation of the newborn rat. Br J Pharmacol 86: 95–104
Nieuwanhuys R, Opdam P (1986) Structure of the brainstem. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, New York, 811–847
Onimaru H, Arata A, Homma I (1988) Primary respiratory rhythm generator in the medulla of the brainstem-spinal cord preparations from newborn rats. Neurosci Lett 78: 151–156
Onimaru H, Arata A, Homma I (1989) Firing properties of respiratory rhythm generating neurons in the absence of synaptic transmission in rat medulla in vitro. Exp Brain Res 76: 530–536
Rovainen CM (1983) Generation of respiratory activity by the lamprey brain exposed to picrotoxin and strychnine, and weak synaptic inhibition in motoneurons. Neuroscience 10: 875–882
Sakakibara Y (1984) The pattern of respiratory nerve activity in the bullfrog. Jpn J Physiol 34: 269–282
Schmidt RS (1973) Central mechanisms of frog calling. Am Zool 13: 1169–1177
Smith JC, Ellenberger HH, Ballanyi K, Richter D, Feldman JL (1991) Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 726–729
Speck DR, Feldman JL (1982) The effects of microstimulation and microlesions in the ventral and dorsal respiratory groups in the medulla of the cat. J Neurosci 2: 744–757
StJohn W (1983) Independent brainstem sites for ventilatory neurogenesis. J Appl Physiol 55: 433–439
Strichartz G (1976) Molecular mechanisms of nerve block by anesthetics. Anesthesiology 45: 421–444
Takeda R, Remmers JE, Baker JP, Farber JP (1986) Postsynaptic potentials of bulbar respiratory neurons of the turtle. Resp Physiol 64: 149–160
West NH, Jones DR (1975) Breathing movements in the frog Rana pipiens. I. The mechanical events associated with lung and buccal ventilation. Can J Zool 53: 332–334
West NH, Topor ZL, van Vliet BN (1987) Hypoxemic threshold for lung ventilation in the toad. Resp Physiol 70: 377–390
Zieglgänsberger W, Puil WA (1973) Actions of glutamic acid on spinal neurones. Exp Brain Res 17: 35–49
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
McLean, H.A., Perry, S.F. & Remmers, J.E. Two regions in the isolated brainstem of the frog that modulate respiratory-related activity. J Comp Physiol A 177, 135–144 (1995). https://doi.org/10.1007/BF00225094
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00225094