Neural Repertoire Behind the World's Most Complex Retina: Neuroanatomy of the Stomatopod Lamina

Abstract

The lamina is the first optic neuropil and visual information integration station in crustaceans and insects, containing synaptic connections between photoreceptors and first-order interneurons. The lamina circuitry in mantis shrimp (stomatopods) is both interesting and complex, as there are 16 different types of photoreceptors contained within the mid-band region of the eye. Using serial block-face scanning electron microscopy, we have reconstructed photoreceptor terminals and lamina interneurons in two major superfamilies with different visual ecologies. Neurons follow the same general pattern as other crustaceans but with notable differences in gross anatomy from insects. The photoreceptors form bulbous terminals in the lamina, following the same overall connectivity pattern in all lamina cartridges across species examined and eye regions. The photoreceptor terminals themselves appear to be complex, with many large mitochondria, a notable difference between insects and stomatopods. Connectivity between photoreceptors and interneurons, as well as cross-cartridge connections, is estimated based on neuronal overlap. Lamina monopolar cells follow previous research in stomatopods and crustaceans, with a set of common neuron types that may provide the beginning of an opponency circuit. Additionally, neurons that extend beyond their parent cartridge in the midband show a preference for branching between rows within the same visual column of cells, as well as some connections within the same row. This added complexity suggests that the stomatopod lamina performs a unique processing of visual signals versus other crustaceans and insects and provides further evidence for the emerging hypotheses around the processing of information by the scanning visual system of stomatopods.