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

Many animals strongly rely on vision, as it provides high-dimensional information about the natural world. 1 To extract relevant features, neural systems filter and categorize the visual input early on to reduce its complexity. 2 In insects, the first visual processing stage of the brain, the lamina neuropil, plays an important role in parallel processing. 3 Its main relay neurons, lamina monopolar cells (LMCs), 4 receive direct photoreceptor input and shape the contrast, luminance, and spatial and temporal tuning of the insect visual system in a cell-type-specific manner. However, how contrast and luminance processing is delineated by LMCs is known only from fruit flies, 5 while the contribution of LMCs to spatial processing has been described in hawkmoths. 6 Here, we reconcile the contrast, luminance, and spatial processing properties of LMCs feeding to the best-investigated downstream target, the motion pathway. 7 To this aim, we provide a novel characterization of hawkmoth LMCs, using serial block-face scanning electron microscopy to reconstruct the anatomical fine structure and connectivity of LMCs in a focal lamina cartridge. We further characterized the functional properties of the main relay neurons (L1 and L2) to the motion pathway in terms of contrast and spatial processing. 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.