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

Abstract

Light-evoked K + flux and intracellular Miiller (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. Miiller cell responses were small but otherwise similar to those recorded in eyecups drained of vitreous. The proximal K + increase and Miiiler cell responses had identical decay times, and on some occasions the latency and rise time of the K + increase nearly matched Mfiller 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 extraceUular 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 lightevoked K + increase that depolarizes glial cells to generate the M-wave.

Neurovascular Coupling Is Not Mediated by Potassium Siphoning from Glial Cells

“…Experimental stimulation resulted in glial cell depolarizations of 40 -100 mV, whereas neuronal activity evoked by light stimulation depolarizes retinal glial cells by ϳ1 mV (Karwoski and Proenza, 1980). Thus, K ϩ efflux evoked experimentally was many-fold greater than efflux evoked by light stimulation.…”

Model Based on Extracellular Potassium for Spontaneous Synchronous Activity in Developing Retinas

“…We justify this simplification because cell body surfaces are separated by approximately 10 11m (Meister et ai. 1991) and K+ ions diffuse in a three-dimensional aqueous medium over this distance in about 8 msec (Hille 1984-21 We modeled active uptake of K+ from the extracellular space by retinal Muller cells (Karwoski and Proenza 1980) by the following secondorder removal differential equation:…”

Transient adaptation and sensitization in the retina of Necturus.

“…With regard to both RD and TRE, we find that [K+]o, extracellular potential, and Miiller-cell membrane potential parallel the changes seen in on/off neurons (see also Karwoski and Proenza [1977, and 1980). It is difficult, however, to determine whether the potential changes seen in on/off neurons are the result or cause of these other changes.…”

“…However, even if such interactions do occur, they would probably be a minor factor in the present results, because there is evidence that Mfillercell depolarizing responses are generated primarily by K + released from on/ off neurons (Karwoski andProenza, 1978 and1980), which themselves show RD and TRE.…”

“…The responses of 18 Mfiller cells, identified by the criteria of Miller and Dowling (1970) and Karwoski andProenza (1977 and1980) were also tested.…”