Functional segregation of retinal ganglion cell projections to the optic tectum of rainbow trout

Abstract

The interpretation of visual information relies on precise maps of retinal representation in the brain coupled with local circuitry that encodes specific features of the visual scenery. In nonmammalian vertebrates, the main target of ganglion cell projections is the optic tectum. Although the topography of retinotectal projections has been documented for several species, the spatiotemporal patterns of activity and how these depend on background adaptation have not been explored. In this study, we used a combination of electrical and optical recordings to reveal a retinotectal map of ganglion cell projections to the optic tectum of rainbow trout and characterized the spatial and chromatic distribution of ganglion cell fibers coding for increments (ON) and decrements (OFF) of light. Recordings of optic nerve activity under various adapting light backgrounds, which isolated the input of different cone mechanisms, yielded dynamic patterns of ON and OFF input characterized by segregation of these two fiber types. Chromatic adaptation decreased the sensitivity and response latency of affected cone mechanisms, revealing their variable contributions to the ON and OFF responses. Our experiments further demonstrated restricted input from a UV cone mechanism to the anterolateral optic tectum, in accordance with the limited presence of UV cones in the dorsotemporal retina of juvenile rainbow trout. Together, our findings show that retinal inputs to the optic tectum of this species are not homogeneous, exhibit highly dynamic activity patterns, and are likely determined by a combination of biased projections and specific retinal cell distributions and their activity states.