The functional morphology of hawkmoth lamina monopolar cells reveals mechanisms of spatial processing in insect motion vision

Many animals strongly rely on their sense of vision, as it provides information about the natural world with particularly high dimensionality. In insects, the first visual processing stage of the brain, the lamina, plays an important role in parallel processing of this complex information. Its main relay neurons, lamina monopolar cells (LMCs), receive information directly from the photoreceptors and shape the contrast, luminance, spatial and temporal tuning of the insect visual system in a cell-type specific manner. One of their best-investigated downstream targets is the motion vision pathway. However, how LMC types that feed into motion processing delineate contrast and luminance is only known from fruit flies, while the contribution of LMCs to spatial processing has only been described in hawkmoths. Here, we provide a novel characterization of hawkmoths lamina monopolar cells, to integrate the contrast, luminance and spatial processing properties of LMCs in the motion pathway. We used serial block-face scanning electron microscopy to reconstruct the anatomical fine structure of LMCs in a focal lamina cartridge, including their pre- and post-synaptic connections. Combining our novel LMC classification with intracellular recordings, we further investigated the functional role of the main relay neurons to the motion pathway, L1 and L2, in terms of contrast and spatial processing. We show that unlike in flies, L1 and L2 process contrast, and spatial information similarly. Crucially, their two distinct spatial processing functions, lateral inhibition and spatial summation are explained by the density and distribution of their synapses in different lamina layers. Based on these findings, we propose a novel mechanism of delineating distinct spatial processing functions in a single cell.