Zebrafish inner retina: local signals for spatial position, luminance, and color contrast

The retina of the zebrafish (Danio rerio) provides an unusually favorable preparation for genetic and developmental studies of the retina. Although the retina has been studied extensively for two decades, the neuronal response of the inner retina is largely unknown. This report describes a prominent local field potential of the inner retina, the Proximal Negative Response (PNR). It is best evoked by small (100 μm) precisely positioned spots of light and is exceedingly sensitive to negative luminance contrast. The polarity, waveform, and other properties of the PNR suggest that it arises primarily from ON-OFF neurons of the proximal retina. The dominant response to negative contrast and its enhancement by light adaptation is believed due to a dominant presynaptic input from OFF bipolar cells. Color contrast was investigated by analyzing responses to a green bar moving on green versus red backgrounds. Over an intermediate range of irradiance, the response to green on red was larger than the response to green on green, thereby providing evidence for the encoding of color contrast. The present findings complement the classic principle of color contrast for human vision known as Kirschmann's third law and bring to mind the view of Walls that color contrast may have been the driving force for the evolution of color vision in lower vertebrates. In sum, the PNR of zebrafish provides clear evidence for the encoding of color and luminance contrast in the inner retina. It exhibits the defining properties common to many other vertebrates, reinforcing the view that the zebrafish may further serve as a model for retinal function and that the PNR may provide a new approach for studies of development, genetics, and retinal degeneration in zebrafish.