Abstract
Respiratory (C3–C5) activity and extracellular K+, pH and Ca2+ (aKe, pHe, [Ca]e, respectively) in the ventral respiratory group (VRG) were measured in vitro. In brainstem-spinal cord preparations from 0- to 1 -day-old rats, lowering of bath glucose content from 30 to 10 mM for 1 h did not affect aKe or rhythmic activity. In preparations from 2- to 3-day-old animals, however, an aKe rise by about 1 mM and disturbance of rhythm occurred after a delay of 50 min. Glucosefree saline resulted, after about 30 min, in reversible blockade of respiratory rhythm and an aKe rise by more than 8 mM, whereas pHe remained unaffected. Exposure to anoxia for 30 min after 1 h of pre-incubation in 10 mM glucose led to a progressive rise of aKe, and a fall of [Ca]e. The concomitant suppression of rhythm was irreversible in preparations from 2- to 3-day-old animals. Similar effects on aKe and [Ca]e and irreversible blockade of rhythm were revealed during anoxia in glucose-free solution, or by addition of 2–5 mM iodoacetate to oxygenated or hypoxic solutions. Iodoacetate led to a slow increase of pHe by more than 0.2 pH units, which was accelerated by anoxia. Our findings show that normal respiratory network functions in the en bloc medulla, in particular from rats older than 1 day, depend on high bath glucose levels, necessary for effective utilization of anaerobic metabolism.
Similar content being viewed by others
References
Ballanyi K, Grafe P, Reddy MM, ten Bruggencate G (1984) Different types of potassium transport linked to carbachol and γ-aminobutyric acid actions in rat sympathetic neurons. Neuroscience 12:917–927
Ballanyi K, Kuwana S, Völker A, Morawietz G, Richter DW (1992) Developmental changes in the hypoxia tolerance of the in vitro respiratory network of rats. Neurosci Lett 148:141–144
Bomont L, Bilger A, Boyet S, Vert P, Nehlig A (1992) Acute hypoxia induces specific changes in local cerebral glucose utilization at different postnatal ages in the rat. Dev Brain Res 66:33–45
Booth RFG, Patel TB, Clark JB (1980) The development of enzymes of energy metabolism in the brain of a precocial (guinea pig) and non-precocial (rat) species. J Neurochem 34:17–25
Brockhaus J, Ballanyi K, Smith JC, Richter DW (1993) Microenvironment of respiratory neurons in the in vitro brainstem-spinal cord of neonatal rats. J Physiol (Lond) 462:421–445
Duffy TE, Kohle SJ, Vannucci RC (1975) Carbohydrate and energy metabolism in perinatal rat brain: relation to survival in anoxia. J Neurochem 24:271–276
Ekholm A, Katsura K, Siesjö BK (1993) Coupling of energy failure and dissipative K+flux during ischemia: role of preischemic plasma glucose concentration. J Cereb Blood Flow Metab 13:193–200
Errchidi S, Monteau R, Hilaire G (1991) Noradrenergic modulation of the medullary respiratory rhythm generation in the newborn rat: an in vitro study. J Physiol (Lond) 443:477–498
Fazekas JF, Alexander FAD, Himwich HE (1941) Tolerance of the newborn to anoxia. Am J Physiol 134:282–287
Feldman JL, Smith JC, Liu G (1991) Respiratory pattern generation in mammals: in vitro en bloc analyses. Curr Opin Neurobiol 1:590–594
Grote J, Zimmer K, Schubert R (1981) Effects of severe arterial hypocapnia on regional blood flow regulation in the brain cortex of cats. Pflügers Arch 391:195–199
Haddad GG, Jiang C (1993) O2 deprivation in the central nervous system: on mechanisms of neuronal response, differential sensitivity and injury. Prog Neurobiol 40:277–318
Hansen AJ (1978) The extracellular potassium concentration in brain cortex following ischemia in hypo- and hyperglycemic rats. Acta Physiol Scand 102:324–329
Hansen AJ (1985) Effect of anoxia on ion distribution in the brain. Physiol Rev 65:101–148
Hochachka PW (1986) Defense strategies against hypoxia and hypothermia. Science 231:234–241
Kawai S, Yonetani M, Nakamura H, Okada Y (1989) Effects of deprivation of oxygen and glucose on the neural activity and the level of high energy phosphates in the hippocampal slices of immature and adult rat. Dev Brain Res 48:11–18
Kuschinsky W, Suda S, Solokoff L (1981) Local cerebral glucose utilization and blood flow during metabolic acidosis. Am J Physiol 241:H772-H777
Lutz PL (1992) Mechanisms for anoxic survival in the vertebrate brain. Annu Rev Physiol 54:601–618
Morawietz G, Ballanyi K, Kuwana S, Richter DW (1995) Oxygen supply and ion homeostasis of the respiratory network in the in vitro perfused brainstem of adult rats. Exp Brain Res 106:265–274
Okada Y, Mückenhoff K, Holtermann G, Acker H, Scheid P (1993) Depth profiles of pH and PO2 in the isolated brain stemspinal cord of the neonatal rat. Respir Physiol 93:315–326
Okada Y, Mückenhoff K, Scheid P (1993) Hypercapnia and medullary neurons in the isolated brain stem-spinal cord of the rat. Respir Physiol 93:327–336
Onimaru H (1995) Studies of the respiratory center using isolated brainstem-spinal cord preparations. Neurosci Res 21: 183–190
Pérez-Pinzón MA, Chan Y, Rosenthal M, Sick TJ (1992) Membrane and synaptic activity during anoxia in the isolated turtle cerebellum. Am J Physiol 263:R1057-R1063
Richter DW, Ballanyi K (1995) Response of the medullary respiratory network to hypoxia: a comparative analysis of neonatal and adult mammals. In: Haddad G, Lister G (eds) Tissue oxygen deprivation: developmental, Molecular and Integrated Function. Dekker, New York 751–777
Siesjö BK (1985) Acid-base homeostasis in the brain: physiology, chemistry, and neurochemical pathology. Prog Brain Res 63:121–154
Suzue T, Murakoshi T, Tamai S (1983) Electrophysiology of reflexes in an isolated brainstem-spinal cord preparation of the newborn rat. Biomed Res 4:611–614
Vannucci RC, Duffy TE (1977) Cerebral metabolism in newborn dogs during reversible asphyxia. Ann Neurol 1:528–534
Vannucci RC, Vannucci SJ (1978) Cerebral carbohydrate metabolism during hypoglycemia and anoxia in newborn rats. Ann Neurol 4:73–79
Völker A, Ballanyi K, Richter DW (1993) Glucose utilization and potassium homeostasis in the in vitro brainstem-spinal cord of neonatal rats (abstract). In: Eisner N, Heisenberg M (eds) Gene-brain. Behaviour. Thieme, Stuttgart, pp 623
Völker A, Ballanyi K, Richter DW (1993) Glucose dependence of ionic homeostasis in the isolated respiratory network of neonatal rats (abstract). Proceedings of the XXXII Congress of the International Union of Physiological Sciences. August 1–6, Glasgow. Proc XXXII IUPS 141.27
Völker A, Ballanyi K, Richter DW (1995) Anoxic disturbance of the isolated respiratory network of neonatal rats. Exp Brain Res 103:9–19
Wong-Riley MTT (1989) Cytochrome oxidase: an endogeneous metabolic marker for neuronal activity. Trends Neuro Sci 12:94–101
Xia Y, Jiang C, Haddad GG (1992) Oxidative and glycolytic pathways in rat (newborn and adult) and turtle brain: role during anoxia. Am J Physiol 262:R595-R603
Zhang E, Hansen AJ, Wieloch T, Lauritzen M (1990) Influence of MK-801 on brain extracellular calcium and potassium activities in severe hypoglycemia. J Cereb Blood Flow Metab 10:136–139
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ballanyi, K., Völker, A. & Richter, D.W. Functional relevance of anaerobic metabolism in the isolated respiratory network of newborn rats. Pflügers Arch. 432, 741–748 (1996). https://doi.org/10.1007/s004240050193
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s004240050193