Extracellular potassium activity, intracellular and extracellular potential responses in the spinal cord

1. Microcapillary electrode assemblies of two or three channels were used to record extracellular and intracellular potentials together with the extracellular activity of potassium ions, from essentially single locations within the substance of the decapitate spinal cord of cats. A liquid ion exchanger filled the tip of the potassium sensing microprobe. Activity was evoked by electrical stimulation of afferent peripheral nerves (ventral roots were cut). 2. Within the substance of the spinal grey matter increments of extracellular potassium activity evoked by repetitive afferent volleys were precisely correlated with magnitudes of sustained shifts of extracellular electric potential. Raising [K+]o from 3 to 4 mM was associated with a negative shift of potential of 2-5 +/- 0-5 mV, regardless of the position of the electrode in the tissue, and regardless of treatment by convulsant or depressant drugs. 3. The spatial distribution of the responses of potassium activity was mapped by the spatial distribution of the negative sustained potential shifts. 4. Depolarization shifts of potential recorded from within neuroglia cells ran parallel with changes of extracellular potassium potential. Even though the magnitude of extracellular sustained potential shifts was precisely correlated with the responses of both extracellular potassium and intracellular glial potentials, the trajectory of sustained potential shifts did not exactly mirror the two other variables. Onset and offset of sustained potential shifts were faster than those of glial potentials or of extracellular potassium. 5. The responses of the true transmembrane potential (intracellular less extracellular potential shifts) of neuroglia cells in the spinal grey matter can fully be described by the Nernst equation. 6. Membrane potentials of neurones, potentials recorded from dorsal root filaments, or from white matter, appeared unrelated to the activity of potassium ions in extracellular fluid. 7. The results are compatible with the suggestions that changes of the membrane potential of spinal neuroglia cells are fully determined by the change of the activity of extracellular potassium, and that glia cells supply most of the current which generates sustained shifts of the extracellular potential of spinal grey matter. The results are hard to reconcile with suggestions that under conditions of moderate excitation (i.e. in the absence of convulsive neuronal activity) changes of extracellular potassium would significantly influence the membrane potential of spinal neurones, or of primary afferent nerve fibres.