1. The light-adapted diffuse-flash electroretinogram (ERG) in the cat exhibits two prominent negative components: a sustained negative potential during illumination and a negative-going OFF response. We investigated their intraretinal origins and found that the sustained component originates from the rod photoreceptors, whereas the OFF response represents a combination of the return to base line of the rod-receptor potential, the offset of PII (rod and cone), and a cone-dependent OFF response originating proximal to the photoreceptors at very high background levels. 2. The ERG, evoked in response to diffuse illumination of the light- and dark-adapted cat retina, was recorded between a chlorided silver wire in the vitreous and a plate behind the eye. Extracellular field potentials were recorded simultaneously with a microelectrode placed intraretinally at different retinal depths. 3. The sustained negative potential and the negative OFF response were not the M-wave ON and OFF responses of proximal retina, despite an overall resemblance in form and time course: 1) the M-wave was spatially tuned, whereas the ERG components were not; 2) tetrodotoxin (TTX) (3.8-microM vitreal concentration) did not alter the M-wave, but it reduced the ERG OFF response; 3) picrotoxin (0.14 mM, after TTX) enhanced the M-wave but did not affect the negative ERG; and 4) 2-amino-4-phosphonobutyric acid (APB; 0.95 mM) removed the M-wave ON response, and aspartate (43 mM) removed the M-wave OFF response, in addition, while the sustained negative potential persisted. 4. The sustained negative potential was not slow PIII, the neural retinal component of the c-wave, a Müller cell response to the photoreceptor-dependent light-evoked decrease in subretinal extracellular K+ concentration [( K+]o). Although Ba2+ (repeated injections of 4-5 mM), a K+ conductance blocker, eliminated slow PIII, it did not remove the sustained negative potential. We concluded that the sustained negative potential was a photoreceptor potential, and the spectral sensitivity of the response indicated that it arose from rods. 5. The contribution of the rod-receptor potential to the ERG depended on background illumination. It was a sustained potential for a range of backgrounds near and 1 or 2 log units above the illumination that saturates rod-driven responses in cat (8.2 log quanta.deg-2.s-1). At lower background intensities, it appeared only as a dip between the b- and c-waves, the b-wave trough, which also was present in fully dark-adapted responses.(ABSTRACT TRUNCATED AT 400 WORDS)