Intracellular recordings were obtained from 57 cone-driven bipolar
cells in the light-adapted retina of the land-phase (adult) tiger
salamander (Ambystoma tigrinum). Responses to flashes of negative
and positive contrast for centered spots of optimum spatial dimensions
were analyzed as a function of contrast magnitude. On average, the
contrast/response curves of depolarizing and hyperpolarizing bipolar
cells in the land-phase animals were remarkably similar to those
of aquatic-phase animals. Thus, the primary retinal mechanisms
mediating contrast coding in the outer retina are conserved as the
salamander evolves from the aquatic to the land phase. To evaluate
contrast encoding in the context of natural environments, the distribution
of contrasts in natural images was measured for 65 scenes. The results, in
general agreement with other reports, show that the vast majority of
contrasts in nature are very small. The efficient coding hypothesis of
Laughlin was examined by comparing the average contrast/response
curves of bipolar cells with the cumulative probability distribution of
contrasts in natural images. Efficient coding was found at 20
cd/m2 but at lower levels of light adaptation, the
contrast/response curves were much too shallow. Further experiments
show that two fundamental physiological factors—light adaptation and
the nonlinear transfer across the cone-bipolar synapse are essential for
the emergence of efficient contrast coding. For both land- and
aquatic-based animals, the extent and symmetry of the dynamic range of the
contrast/response curves of both classes of bipolar cells varied
greatly from cell to cell. This apparent substrate for distributed
encoding is established at the bipolar cell level, since it is not found
in cones. As a result, the dynamic range of the bipolar cell population
brackets the distribution of contrasts found in natural images.