Relationship between neuronal activity and extracellular potassium during seizure in the ventrobasal thalamus of the cat

Extracellular potassium concentration ((K⁺)₀) and neuronal activities were simultaneously recorded in the specific thalamic nucleus Ventralis Posterolateralis (VPL) using double-barrelled, ion-sensitive microelectrodes. Resting levels of thalamic (K⁺)₀ were between 2.7 and 3.2 in mM/1. During repetitive stimulation of the contralateral cuneate nucleus, (K⁺)₀ never increased by more than 0.7 mM/l. However, repetitive stimulation of the ipsilateral primary sensorimotor cortex, or underlying white matter caused thalamic (K⁺)₀ to increase to levels as high as 12 mM/l. Similar increases were observed during transition from interictal to ictal activity in penicillin-induced cortical epileptogenic foci. These large changes in (K⁺)₀ were closely related to generation of high-frequency bursts of action potentials in thalamocortical relay (TCR) neurons. During the course of a propagated seizure, (K⁺)₀ gradually fell from the peak level. At the conclusion of the seizure, neuronal bursting abruptly ceased, and (K⁺)₀ rapidly decayed to below the baseline level. During the decay in (K⁺)₀, negative thalamic field potentials evoked by afferent stimuli were increased in amplitude, and the safety factor for antidromic invasion of TCR neurons by cortically-evoked action potentials was markedly reduced. These results suggest that seizure termination is associated with hyperpolarization of thalamic neurons, which may be due to activation of an electrogenic pump mechanism.