Neurons, potassium, and glia in proximal retina of Necturus.

Abstract

Light-evoked K+ flux and intracellular Müller (glial) cell and on/off-neuron responses were recorded from the proximal retina of Necturus in eyecups from which the vitreous was not drained. On/off-responses, probably arising from amacrine cells, showed an initial transient and a sustained component that always exhibited surround antagonism. Müller cell responses were small but otherwise similar to those recorded in eyecups drained of vitreous. The proximal K+ increase and Müller cell responses had identical decay times, and on some occasions the latency and rise time of the K+ increase nearly matched Müller cell responses, indicating that the recorded K+ responses were not always appreciably degraded by electrode "dead space." The spatiotemporal distribution of the K+ increase showed that both diffusion and active reuptake play important roles in K+ clearance. The relationship between on/off-neuron responses and the K+ increase was modelled by assuming that (a) K+ release is positively related to the instantaneous amplitude of the neural response, and (b) K+ accumulating in extracellular space is cleared via mechanisms with approximately exponential time-courses. These two processes were approximated by low-pass filtering the on/off-neuron responses, resulting in modelled responses that match the wave form and time-course of the K+ increase and behave quantitatively like the K+ increase to changes in stimulus intensity and diameter. Thus, on/off-neurons are probably a primary source of the proximal light-evoked K+ increase that depolarizes glial cells to generate the M-wave.