Changes in extracellular potassium concentration in cortex and brain stem during the acute phase of experimental closed head injury

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✓ A high potassium concentration ([K+]o) in brain tissue impedes neuronal activity, as observed in spreading cortical depression. Experimental studies were performed on mice and rats to determine the role of changes of [K+]o in cerebral concussion. In the first experiment, a 600 gm-cm impact was delivered to the vertex of the mouse skull. This impact induced arrest of spontaneous movement for 465 ± 55.9 seconds (mean ± SD), accompanied by apnea, bradycardia, and low-voltage electroencephalographic recordings (EEG). The injury was also frequently followed immediately by epilepsy. This impact induced an increase of cortical [K+]o from the control level of 4.1 ± 1.8 mM to 20–30 mM, with gradual recovery within 30 minutes to the control level.

In the second experiment, an impact of 9000 gm-cm was delivered to the midline parieto-occipital area of the rat and produced concussion-like phenomena similar to those elicited in mice. This level of trauma induced a significant increase of cortical [K+]o from the control level of 4.2 ± 0.8 mM to 20–50 mM in all of the rats, and also a significant increase of brain-stem [K+]o from 3.9 ± 0.6 to 20–30 mM in 73% of the rats. In these latter rats, the impact also induced apnea and a transient elevation of blood pressure, and resulted in low-voltage EEG recordings. In 23% of the rats in which [K+]o changes in the brain stem were not significant, the impact caused a transient reduction of blood pressure. The present study disclosed that an increase of [K+]o in the cerebral cortex and also in the brain stem is an important element in the phenomenon of concussion.

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Address reprint requests to: Hiroshi Takahashi, M.D., Department of Neurosurgery, University of Tokyo Hospital, Hongo 7-3-1, Bunkyo-ku, Tokyo, Japan.

© AANS, except where prohibited by US copyright law.

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    Diagram of the set-up in the mouse experiments. Parameters monitored included potassium (K+) concentration and respiration. Electroencephalographic (EEG) and electrocardiographic (EKG) data were also obtained.

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    Left: Diagram of the set-up in the rat experiments. Parameters monitored included potassium (K+) concentration and respiration. Electroencephalographic (EEG) and electrocardiographic (EKG) data were also obtained. Right: The track of the potassium (K+)-sensitive electrode in the brain stem is shown. Some contusion is seen on the cortex where the electrode was inserted, but there are no overt pathological findings in the brain stem.

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    Changes of cortical potassium concentration ([K+]o) and in the electroencephalographic (EEG) recording following an impact with 600 gm-cm to the vertex of the skull of Mouse 18. Control [K+]o was about 3 mM. Immediately after impact, [K+]o increased to about 25 mM, followed by gradual recovery. Thirty minutes after impact, the animal was sacrificed with pentobarbital (Nembutal), and [K+]o rose again to about 50 mM.

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    Summary of the changes of all parameters following an impact of 600 gm-cm to the skulls of 28 mice. The abscissa represents time (minutes) after impact. Changes in potassium concentration ([K+]o) are shown with mean values and standard deviations. Electroencephalographic (EEG) changes are demonstrated with mean frequency (counts/sec) and standard deviation, and also with the amplitude changes of every frequency component (delta to beta): 100 represents 50 mV (ordinate). Pulse and respiratory rates are expressed per minute. Immediately after the impact, [K+]o increased, amplitudes of frequency components of the EEG decreased, and pulse and respiratory rates also decreased transiently. Significance: • = p < 0.05; ** = p < 0.01.

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    Spreading cortical depression was elicited in a rat by the topical application of KCl (100 mM) on the cortex with filter paper. Only the cortical potassium concentration ([K+]o) increased markedly. B.S. = brain stem.

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    Summary of changes of all parameters in Type I animals (left) and Type II animals (right). Changes are demonstrated with mean value and standard deviation. [K+]o = potassium concentration; EEG = electroencephalogram. Significance: • = p < 0.05; ** = p < 0.01.

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    Example of a Type I animal (Rat 9). Potassium concentration ([K+]o) in the cortex, [K+]o in the brain stem (B.S.), respiration, blood pressure (BP), and electroencephalogram (EEG) are demonstrated. Immediately after impact with 9000 gm-cm to the parieto-occipital area of this rat, apnea, elevated BP, and low-voltage EEG appeared. At this time, [K+]o in the cortex was about 40 mM, and [K+]o in the brain stem was about 25 mM; gradual recovery of each parameter ensued.

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    Example of a Type II animal (Rat 11). Abbreviations are the same as in Fig. 7. After impact, cortical [K+]o remained high, but brain-stem [K+]o showed recovery.

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    Summary of changes in all parameters in each Type III animal (left) and in all Type IV animals (right) in which changes are demonstrated with mean value and standard deviation. [K+]o = potassium concentration; EEG = electroencephalogram. Significance: * = p < 0.05.

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    Example of a Type III animal (Rat 19). Abbreviations are the same as in Fig. 7. Directly after impact, BP decreased and EEG became almost flat; temporary hyperventilation was observed.

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    Example of a Type IV animal (Rat 23). Abbreviations are the same as in Fig. 7. The [K+]o in the brain stem (B.S.) was about 8 mM after impact. Blood pressure (BP) became temporarily lower.

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