A novel computation for dimming relative to the adaptation level in the frog retina

Ambient luminance varies widely, and retinal output is shaped by adaptation-dependent gain control. Relative to the adaptation level, a decrease in light intensity can either return intensity toward the adaptation level or drive it farther away from that level. Whether OFF retinal outputs signal both changes simply as light-intensity decrements or distinguish them according to their relationship to the adaptation level is currently unclear. This study examined OFF sustained retinal ganglion cells in bullfrogs (Rana catesbeiana) of either sex and quantified response bias by comparing spike counts during decrements that moved toward and away from the adaptation level. Responses fell into two functional populations: one signaled decrements in both cases, whereas the other selectively signaled decrements that moved away from the adaptation level, indicating adaptation level-referenced encoding. Although surround suppression was considered a possible contributor to these differences, manipulations expected to reduce classical surround contributions did not explain the selective suppression of responses during decrements that moved toward the adaptation level. Blocking GABA_A receptors (GABA_ARs) consistently weakened the response asymmetry between decrements that moved toward and away from the adaptation level, suggesting that GABA_AR-dependent inhibition contributes to the mechanism underlying adaptation level-referenced responses. Taken together, these findings reveal a distinct computation for light-intensity decrement processing and expand the functional diversity of OFF outputs across light-intensity contexts.Significance statement This study reveals functional diversity among OFF sustained retinal ganglion cells (RGCs) in frogs in how they encode light-intensity decrements relative to the adaptation level. Rather than simply reporting decrements, cells fell into two functional groups: one responded to decrements that moved toward and away from the adaptation level, whereas the other selectively responded to decrements that moved away from the adaptation level. This distinction indicates that these OFF-retinal outputs encode light-intensity decrements according to their relationship to the current visual context. These findings identify adaptation level-referenced responses in OFF sustained RGCs as a previously unrecognized form of OFF pathway processing.