Simultaneous recording of local electrical activity, partial oxygen tension and temperature in the rat hippocampus with a chamber-type microelectrode. Effects of anaesthesia, ischemia and epilepsy

A miniature multiple thin-film recording sensor was used to measure simultaneously the electrical activity, oxygen content and temperature of brain tissue. The chamber-type potential sensor was an Ag/AgCl electrode covered by an Si3N4 (silicon nitride) chamber. The chamber-type oxygen sensor consisted of an Au-Ag/AgCl two-electrode electrochemical cell embedded in an electrolyte-filled Si3N4 chamber. The temperature sensor was a thin-film germanium resistor. The different sensors were spaced 300 microns apart. Anaesthetics (pentobarbital, chloral hydrate, chlornembutal, halothane) were shown to depress electrical activity and to increase local oxygen tension in the hippocampus. Halothane, but not the other anaesthetics, also increased the current output of the oxygen sensor when tested in saline bath, indicating that the apparent increase in measured oxygen levels during halothane anaesthesia was partly due to an electrochemical effect of halothane on the oxygen sensors. The decrease of tissue oxygen consumption produced by the other anaesthetics is likely to be the result of metabolic depression. Cerebral ischemia, evoked by cauterization of the vertebral arteries and occlusion of the carotid arteries for 30 min, resulted in the disappearance of both spontaneous and evoked electrical activity in the hippocampus and a decrease of both local temperature and oxygen tension. There was a marked overshoot of the oxygen tension to above preocclusion level following the release of the carotid arteries. As soon as electrical activity returned, the oxygen tension fell again, often below the lowest level seen during the ischemic period. This secondary decrease of oxygen level could be reversed by administration of supplementary small doses of anaesthetic. The anaesthetic-induced increase in oxygen tension was accompanied by a marked decrease in electroencephalogram amplitude and frequency. During electrically induced seizures a decrease in hippocampal oxygen content occurred and was accompanied by an increase of local temperature. Since the rectal temperature was kept constant, the changes in temperature are likely to reflect changes in blood perfusion of the recorded area. These findings are in agreement with previous observations made with conventional electrodes. In addition, the miniature size of the chamber-type microelectrode assembly allows a correlated monitoring of parallel physiological changes with high spatial and temporal resolution during anaesthesia, ischemia and epilepsy.

[1]  J. Seylaz,et al.  Local cerebral PO2, PCO2, and blood flow measurements by mass spectrometry. , 1983, The American journal of physiology.

[2]  J. Brierley,et al.  A New Model of Bilateral Hemispheric Ischemia in the Unanesthetized Rat , 1979, Stroke.

[3]  G. Porro,et al.  Brain energy metabolism in hepatic coma. , 1906, Experimental biology and medicine.

[4]  K. Hossmann,et al.  Relationship between metabolic recovery and the EEG prolonged ischemia of cat brain. , 1986, Stroke.

[5]  C. Nitsch,et al.  Incongruence of regional cerebral blood flow increase and blood-brain barrier opening in rabbits at the onset of seizures induced by bicuculline, methoxypyridoxine, and kainic acid , 1985, Journal of the Neurological Sciences.

[6]  Y. Ben‐Ari,et al.  Blood flow compensates oxygen demand in the vulnerable ca3 region of the hippocampus during kainate-induced seizures , 1984, Neuroscience.

[7]  O. Prohaska,et al.  Thin-Film Multiple Electrode Probes: Possibilities and Limitations , 1986, IEEE Transactions on Biomedical Engineering.

[8]  G. Buzsáki,et al.  Hippocampal responses evoked by tooth pulp and acoustic stimulation: Depth profiles and effect of behavior , 1986, Brain Research.

[9]  Katsuharukimoto,et al.  Cerebral Uptake of Glucose and Oxygen in the Cat Brain After Prolonged Ischemia , 1976 .

[10]  J. Michenfelder,et al.  The Effect of Halothane on Canine Cerebral Metabolism , 1968, Anesthesiology.

[11]  G. Buzsáki,et al.  Cellular bases of hippocampal EEG in the behaving rat , 1983, Brain Research Reviews.

[12]  D. Riche,et al.  Continuous determination of the cerebrovascular changes induced by bicuculline and kainic acid in unanaesthetized spontaneously breathing rats , 1987, Neuroscience.

[13]  L. Kellényi,et al.  Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: Current-source density analysis, effects of urethane and atropine , 1986, Brain Research.

[14]  M. Ingvar,et al.  Local blood flow and glucose consumption in the rat brain during sustained bicuculline‐induced seizures , 1983, Acta neurologica Scandinavica.

[15]  D. Bruley,et al.  Effect of microcirculation changes on brain tissue oxygenation , 1971, The Journal of physiology.

[16]  D. Lampard,et al.  Local Cerebral Blood Flow Following Transient Cerebral Ischemia: I. Onset of Impaired Reperfusion within the First Hour Following Global Ischemia , 1980, Stroke.

[17]  D. Lampard,et al.  Local Cerebral Blood Flow Following Transient Cerebral Ischemia: II. Effect of Arterial Pco2 on Reperfusion Following Global Ischemia , 1980, Stroke.

[18]  W. Pulsinelli,et al.  Regional Energy Balance in Rat Brain After Transient Forebrain Ischemia , 1983, Journal of neurochemistry.

[19]  T. Wieloch Neurochemical correlates to selective neuronal vulnerability. , 1985, Progress in brain research.

[20]  H. Bicher Brain oxygen autoregulation: a protective reflex to hypoxia? , 1974, Microvascular research.

[21]  J. Winson,et al.  Neuronal transmission through hippocampal pathways dependent on behavior. , 1978, Journal of neurophysiology.

[22]  David E. Levy,et al.  Delayed postischemic hypoperfusion , 1979, Neurology.

[23]  K. Hossmann,et al.  Pial Artery Pressure after One Hour of Global Ischemia , 1987, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[24]  H. Eichenbaum,et al.  Unit activity, evoked potentials and slow waves in the rat hippocampus and olfactory bulb recorded with a 24-channel microelectrode , 1985, Neuroscience.

[25]  Ian Q. Whishaw,et al.  Generators and topography of hippocampal Theta (RSA) in the anaesthetized and freely moving rat , 1976, Brain Research.

[26]  B. Siesjö,et al.  Brain energy metabolism , 1978 .

[27]  J. Seylaz,et al.  Continuous measurement of gas partial pressures in intracerebral tissue. , 1978, Journal of applied physiology: respiratory, environmental and exercise physiology.

[28]  C. Liu,et al.  A Thick-Film Multiple Component Cathode Three-Electrode Oxygen Sensor , 1986, IEEE Transactions on Biomedical Engineering.

[29]  J. LaManna,et al.  Cerebral oxygenation during recurrent seizures. , 1983, Advances in neurology.

[30]  P. Picozzi,et al.  Reperfusion after cerebral ischemia: influence of duration of ischemia. , 1986, Stroke.

[31]  R. Weiskopf,et al.  Oxygen electrode errors due to polarographic reduction of halothane. , 1971, Journal of applied physiology.

[32]  E. Speckmann,et al.  Cerebral pO2, pCO2 and pH: Changes During Convulsive Activity and their Significance for Spontaneous Arrest of Seizures , 1972, Epilepsia.

[33]  D. Bruley,et al.  Brain oxygen supply and neuronal activity under normal and hypoglycemic conditions. , 1973, The American journal of physiology.

[34]  L. Symon,et al.  Measurements of oxygen tension in the cerebral cortex of baboons , 1976, Journal of the Neurological Sciences.

[35]  M. Kuperstein,et al.  A Practical 24 Channel Microelectrode for Neural Recording in Vivo , 1981, IEEE Transactions on Biomedical Engineering.

[36]  H. Caspers,et al.  Actions of hypoxia and hypercapnia on single mammalian neurons. , 1973, Advances in experimental medicine and biology.

[37]  W. Pulsinelli,et al.  Regional cerebral blood flow and glucose metabolism following transient forebrain ischemia , 1982, Annals of neurology.

[38]  J. Winson,et al.  Patterns of hippocampal theta rhythm in the freely moving rat. , 1974, Electroencephalography and clinical neurophysiology.

[39]  W. Dalton Dietrich,et al.  Small Differences in Intraischemic Brain Temperature Critically Determine the Extent of Ischemic Neuronal Injury , 1987, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[40]  T. Wieloch,et al.  Ischemic Brain Damage in Rats following Cardiac Arrest Using a Long-Term Recovery Model , 1985, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[41]  J D Michenfelder,et al.  The Nonlinear Responses of Cerebral Metabolism to Low Concentrations of Halothane, Enflurane, Isoflurane, and Thiopental , 1977, Anesthesiology.

[42]  J Astrup,et al.  Oxygen and glucose consumption related to Na+-K+ transport in canine brain. , 1981, Stroke.

[43]  D. Lübbers,et al.  Behavior of microflow and local PO2 of the brain cortex during and after direct electrical stimulation. A contribution to the problem of metabolic regulation of microcirculation in the brain. , 1976, Pflügers Archiv: European Journal of Physiology.

[44]  D. Buerk,et al.  Comparisons of oxygen metabolism and tissue PO2 in cortex and hippocampus of gerbil brain. , 1987, Stroke.

[45]  F Plum,et al.  Cerebral metabolic and circulatory responses to induced convulsions in animals. , 1968, Archives of neurology.

[46]  J. Halsey,et al.  A critical evaluation of oxygen disappearance during stop flow in the gerbil brain. , 1982, Neurological research.

[47]  M. Kameyama,et al.  A new model of bilateral hemispheric ischemia in the rat--three vessel occlusion model. , 1985, Stroke.

[48]  L. Symon,et al.  pH, K+, and PO2 of the Extracellular Space during Ischaemia of Primate Cerebral Cortex , 1987, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[49]  P Andersen,et al.  Entorhinal activation of dentate granule cells. , 1966, Acta physiologica Scandinavica.

[50]  R. S. Pickard Printed circuit microelectrodes , 1979, Trends in Neurosciences.

[51]  D. Mcdowall The effects of clinical concentrations of halothane on the blood flow and oxygen uptake of the cerebral cortex. , 1967, British journal of anaesthesia.