1. In the Necturus retina, light-evoked field potentials, Müller (glial) cell responses, and extracellular potassium ion concentration ([K+]0) were recorded and found to exhibit the three-way correlation characteristic of these variables elsewhere in the nervous system. 2. Müller cell responses to a flashed spot or annulus consist primarily of slow depolarizations at both light onset and offset. The responses are maximum to 0.5-mm-diameter spots and decrease with larger diameters. Responses to stimulus intensity and flicker were also used to characterize Müller cell behavior. 3. In response to long-duration stimuli, the initial Müller cell depolarization is followed by a very slow hyperpolarization, which is likely the origin of slow PIII. 4. A new extracellular potential is described, the M-wave, the basic properties of which suggest that it is generated by Müller cells. Moreover, the M-wave and Müller cells show remarkably similar behavior to a wide variety of stimulus parameters. 5. In the proximal retina, [K+]0 increases at both light onset and offset with a time course similar to that of Müller cell depolarizing responses. This K+ increase also behaves similarly to the Müller cell depolarization in response to changes in stimulus parameters. 6. It is concluded that light stimulation leads to an increase in [K+]0 in the proximal retina and that this increase depolarizes Müller cells whose associated currents, in turn, generate the M-wave.
Measurements of absolute transretinal resistance and of the relative resistance of the various retinal layers were obtained in the frog. The resistance of clamped sections of isolated retina was 66 omega . cm2, which results in an average resistivity (rho) between inner and outer limiting membranes of 5,050 omega . cm. In eyecups, relative resistances (obtained by passing constant currents across the retina) were assigned to specific layers of the retina with the aid of physiological criteria (e.g., depths of light-evoked field potentials, changes in extracellular K+ concentration, base-line noise level, and resistance). These relative resistances were then converted to absolute values, a calculation feasible because the region between inner and outer limiting membranes, which has the same structure in both isolated and eyecup retinas, could be specified during experiments. Resistivities (in omega . cm) for the retinal layers include 1) subretinal space, 970; 2) inner and outer nuclear layers, 6,800; and 3) inner plexiform layer, 1,750. The ganglion cell and optic nerve fiber layers were too thin to resolve individually, but rho of the two layers combined was 7,900. The outer plexiform layer was also too thin to reliably resolve, but its rho is likely the same as the inner plexiform layer. The extracellular space volume fraction (alpha) of the retinal layers was estimated from these rho s, and the following values were obtained: 1) subretinal space, 0.12; 2) outer and inner nuclear layers, 0.03; 3) inner and outer plexiform layers, 0.11; and 4) ganglion cell and optic nerve fiber layers, 0.02. The decreased rho and increased alpha of the inner plexiform layer and the subretinal space, compared with that of the nuclear layers, are expected from their anatomy. A consideration of these inhomogeneities is required in analyses of field potentials and of changes in extracellular ionic concentrations.
Recordings of light-evoked changes in extracellular K+ concentration (A[K+]o) were obtained in the retinas of frog and mudpuppy . In eyecup preparations, various recording approaches were used and provided evidence for a K increase near the outer plexiform layer (distal K increase). This distal K increase could be pharmacologically dissociated from the well-known, large K increase in the proximal retina by the application of ethanol and -y-aminobutyric acid . The distal K increase also often showed surround antagonism . A retinal slice preparation was used to permit electrode placement into the desired retinal layers under direct visual control and without the risk of electrode damage to adjacent layers . In the slice, a distinct distal K increase was found in the outer plexiform layer, in addition to the prominent K increase in the inner plexiform layer. Compared with eyecups, only weak K increases were found in the nuclear layers of the slice. This suggests that the K responses observed in the nuclear layers of eyecups may be generated by K' diffusing along the electrode track from the plexiform layers. In the context of current models of ERG b-wave generation, the magnitude of the recorded distal K increase, compared with the proximal K increase, seems too small to give rise to the bwave . However, the distal K increase may be differentially depressed by electrode dead space. It is also possible that if certain aspects of the models of bwave generation were modified, then the observed distal K increase could give rise to the b-wave .
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.
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