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

Abstract

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.

Effects of concussion on the blood–brain barrier in humans and rodents

“…Additionally, a medical diagnosis of post-concussive syndrome (PCS), which refers to signs and symptoms frequently seen post mild head injury, can differentiate concussion from mTBI; however, the pathogenesis of PCS is not known. 33 It is well known that concussive forces can have a multitude of neurological sequelae, including ionic fluxes (rodent), 34 indiscriminate neuroparenchymal glutamate release (rodent), 35 hyperglycolysis (rodent), 36 lactate accumulation (rodent), 37,38 and diffuse axonal injury (cat, human). [39][40][41] Secondary consequences include intracellular hypercalcemia (rodent), [42][43][44] mitochondrial dysfunction (rodent), 45,46 impaired oxidative metabolism (cat), 47 decreased glycolysis (rodent), 48 diminished cerebral blood flow (rodent), 49,50 axonal disturbances, neurotransmitter disarray, and apoptotic delay.…”

Pretreatment with Phencyclidine, an N-Methyl-d-Aspartate Antagonist, Attenuates Long-Term Behavioral Deficits in the Rat Produced by Traumatic Brain Injury

“…Since 1878 (Duret), investigators have recognized that acute manifestations of TBI include excitation, which is a prerequisite for widespread neurotransmitter release. Recent indirect evidence indicating that TBI can produce widespread neural excitation and depolarization includes increased cerebral blood flow (DeWitt et al, 1986), muscle hypertonia and desynchronous electroencephalographic (EEG) findings , increased oxidation of mitochondrial cytochromes (Duckrow et al, 1981), and increases in extracellular potassium (Takahashi et al, 1981;DeSalles et al, 1988). Other research indicates that TBI can liberate significant amounts of unbound acetylcholine that are detectable in cerebrospinal fluid (Bornstein, 1946;Ruge, 1954;Sachs, 1957; for review see Hayes et al, 1988b).…”

Hippocampal CA3Lesion Prevents Postconcussive Metabolic Dysfunction in CA1

“…Immediately following cerebral concussion there is a marked increase of extracellular potassium (Takahashi et al, 1981;Katayama et al, 1990), a decrease in magnesium Vink et al, 1988), as well as an accumulation of calcium (Ca 2 + ) (Cortez et al, 1989;Thomas et aI. , 1990).…”