Neuronal Interactions Mediated by Neurally Evoked Changes in the Extracellular Potassium Concentration

Neuronal interactions mediated by alteration of the extracellular K+ concentration [K+]o occur between populations as well as among single neurones in very restricted regions. The interactions mediated by K+ ions may range from low efficacy ones (in which the effects of increased [K+]o around the non-active cells can be recorded only after massive activity of a large population of neurones) to very effective interactions (in which a single action potential in a neurone is sufficient to produce a depolarization of several mV in a second one). Such efficient K+-mediated interactions cannot be unequivocally distinguished by shape, amplitude or time course from postsynaptic responses induced by chemical or electrotonic synapses. We review here experiments which demonstrate various levels of interactions mediated by changes in potassium ion concentration. The giant axons (Gax) and non-giant axons from the central nervous system of the cockroach Periplaneta americana were used. The types of interactions discussed are: pathological interactions among populations of neurones induced by the convulsant drug picrotoxin; restricted and limited interactions which are the consequence of the combination of the special geometry of Gaxs and increases in extracellular K+; and finally, local and efficient interactions among Gaxs which are postulated to be mediated by K+ ions. The experiments described in this review, as well as others, demonstrate that the extracellular spaces in the CNS serve as predetermined pathways for K+-mediated neuronal communication. When the extracellular space between two adjacent neurones is very small, the K+-mediated interaction may resemble the PSPs of chemical or electrotonic synapses. It is possible that because of this resemblance, other K+-mediated interactions in the CNS have not been identified as such.