Light-evoked changes in [K+]o in proximal portion of light-adapted cat retina

1. The M-wave is a light-adapted response of proximal retina consisting of phasic negative field potentials at light onset and offset that are spatially tuned for small stimuli. We measured light-dependent changes in extracellular K+ concentration ([K+]o) in proximal retina to investigate the hypothesis that the M-wave originates from Muller cell responses to changes in [K+]o. 2. Extracellular field potentials, and changes in [K+]o evoked in response to circular spots of light flashed on steady backgrounds, were recorded with double-barreled K(+)-sensitive electrodes placed in the retina at different depths. 3. Increases in [K+]o during illumination and at light offset were maximal in proximal retina, with the On [K+]o increase located more proximally than the Off increase. The [K+]o increase during illumination consisted of a phasic and sustained response, whereas the Off [K+]o increase was predominantly phasic. The spatial tuning of the [K+]o increases was similar to the tuning of the field potentials. 4. The Off-field potential was larger than the On potential; it tended to be maximal more distally and was more sharply localized in retinal depth. Stimulus-response characteristics of the field potentials were not altered by intravitreal tetrodotoxin (TTX; 3.8 microM) sufficient to block retinal ganglion cell action potentials. 5. There were no rod contributions to the proximal [K+]o increases and field potentials recorded at the background illuminations used in this study (9.5-11.5 log q.deg-2.s-1). 6. An intravitreal injection of L- or DL-2-amino-4-phosphonobutyric acid (APB; 1 mM) was used to block On-system neuronal responses in proximal retina and isolate Off-system responses. After APB the [K+]o response consisted of a sustained decrease in [K+]o during illumination followed by an overshoot at light offset, while the field potential was a sustained positive response at light onset followed by an initially phasic negative response at light onset followed by an initially phasic negative response at light offset. These responses retained spatial tuning. To isolate the On-system components, the APB-isolated responses were subtracted from the controls. The [K+]o response now consisted of a sustained increase during illumination followed by an undershoot at light offset. The field potential was a sustained negative potential with an initial phasic peak that decayed at Off. Results with kynurenate (KYN; 5 mM) and (+/-)cis-2,3-piperidine (PDA; 5 mM) confirmed the sustained nature of the On component.(ABSTRACT TRUNCATED AT 400 WORDS)