Extracellular K+ accumulation during penicillin-induced epileptogenesis in the CA3 region of immature rat hippocampus.

Ion-selective microelectrode techniques were used to study extracellular K+ changes associated with penicillin-induced epileptogenesis in the CA3 region of hippocampal slices. Recordings were made in slices taken from rats 9-16 days of age, which have a pronounced capacity to undergo prolonged synchronized afterdischarges. Direct comparisons were made to slices from hippocampus from more mature rats, 30-35 days old, which are much less prone to seizure-like events. The amplitude and time course of the K+ transients varied across the CA3 laminae. K+ signals were largest close to stratum pyramidale in stratum oriens (the infrapyramidal zone). Recordings from this site showed extracellular K+ accumulation to be unusually large in immature hippocampus. The ceiling [K+]o level recorded during seizure-like events ranged from 14.4 to 20.2 mM and averaged 16.9 mM. The peak amplitude of extracellular K+ transients following an epileptiform burst in slices from immature rats averaged 4.31 mM while the mean of similar recordings from mature rats was 0.97 mM. Detailed laminar distribution studies in developing hippocampus revealed that the K+ signals were large in the proximal two-thirds of the basilar dendrites and proximal half of the apical dendrites. K+ accumulation in stratum pyramidale was comparatively small even though at its very edge in stratum oriens large K+ transients were always recorded. The latter was also true in recordings from mature hippocampus. Other dendritic signals in mature tissue were comparatively small. Laminar analysis was performed of the field potentials recorded by the reference barrel of the K+ electrodes. Negative field potential for the epileptiform burst and subsequent slow potential correlated in space with sites of K+ accumulation in both immature and mature hippocampal slices. Interictal and prolonged ictal-like discharges, recorded in developing hippocampus, arose from the same baseline [K+]o. However, since [K+]o is excessively high during the course of these epileptiform events it most likely has a role in the unusual propensity of immature hippocampus for seizures.