Multiple spectral channels in branchiopods. I. Vision in dim light and neural correlates

Abstract

Animals that have true color vision possess several spectral classes of photoreceptors. Pancrustaceans (Hexapoda+Crustacea) that integrate spectral information about their reconstructed visual world do so from photoreceptor terminals supplying their second optic neuropils, with subsequent participation of the third (lobula) and deeper centers (optic foci). Here, we describe experiments and correlative neural arrangements underlying convergent visual pathways in two species of branchiopod crustaceans that have to cope with a broad range of spectral ambience and illuminance in ephemeral pools, yet possess just two optic neuropils, the lamina and the optic tectum. Electroretinographic recordings and multimodel inference based on modeled spectral absorptance were used to identify the most likely number of spectral photoreceptor classes in their compound eyes. Recordings from the retina provide support for four color channels. Neuroanatomical observations resolve arrangements in their laminas that suggest signal summation at low light intensities, incorporating chromatic channels. Neuroanatomical observations demonstrate that spatial summation in the lamina of the two species are mediated by quite different mechanisms, both of which allow signals from several ommatidia to be pooled at single lamina monopolar cells. We propose that such summation provides sufficient signal for vision at intensities equivalent to those experienced by insects in terrestrial habitats under dim starlight. Our findings suggest that despite the absence of optic lobe neuropils necessary for spectral discrimination utilized by true color vision, four spectral photoreceptor classes have been maintained in Branchiopoda for vision at very low light intensities at variable ambient wavelengths that typify conditions in ephemeral freshwater habitats.