Representation of the stomatopod's retinal midband in the optic lobes: Putative neural substrates for integrating chromatic, achromatic and polarization information

Abstract

Stomatopods have an elaborate visual system served by a retina that is unique to this class of pancrustaceans. Its upper and lower eye hemispheres encode luminance and linear polarization while an equatorial band of photoreceptors termed the midband detects color, circularly polarized light and linear polarization in the ultraviolet. In common with many malacostracan crustaceans, stomatopods have stalked eyes, but they can move these independently within three degrees of rotational freedom. Both eyes separately use saccadic and scanning movements but they can also move in a coordinated fashion to track selected targets or maintain a forward eyestalk posture during swimming. Visual information is initially processed in the first two optic neuropils, the lamina and the medulla, where the eye's midband is represented by enlarged regions within each neuropil that contain populations of neurons, the axons of which are segregated from the neuropil regions subtending the hemispheres. Neuronal channels representing the midband extend from the medulla to the lobula where populations of putative inhibitory glutamic acid decarboxylase-positive neurons and tyrosine hydroxylase-positive neurons intrinsic to the lobula have specific associations with the midband. Here we investigate the organization of the midband representation in the medulla and the lobula in the context of their overall architecture. We discuss the implications of observed arrangements, in which midband inputs to the lobula send out collaterals that extend across the retinotopic mosaic pertaining to the hemispheres. This organization suggests an integrative design that diverges from the eumalacostracan ground pattern and, for the stomatopod, enables color and polarization information to be integrated with luminance information that presumably encodes shape and motion.

The reniform body: An integrative lateral protocerebral neuropil complex of Eumalacostraca identified in Stomatopoda and Brachyura

“…(a) The right lateral protocerebrum (LPR) immunostained using anti‐α‐tubulin (magenta), anti‐TH (cyan) with neuronal cell bodies stained using Syto13. Anti‐TH resolves systems of through‐going and tangential processes associated with the optic lobe's representation of the retinal midband, such as the medulla midband protuberance (MMP; see, Thoen, et al, ). Anti‐TH also resolves part of one of the mushroom body columnar lobes (Clm).…”

“…These correspond to systems of synaptic baskets (see Section 3), the formations of which are so prominent as to be visible as outswellings from the reniform body surface (Figure a, b). Immunostaining with the synaptic marker SYNORF1 and low power confocal scanning of the whole lateral protocerebrum reveals these features as prominently as it does the medulla's midband protuberance, representing the compound eyes' retinal midband (Thoen et al, ). The dense covering of the calyces by the mushroom body's globuli cells is also shown in Figure a.…”

“…The study by Wolff et al () also provides a brief description of the stomatopod reniform body, comparing it to an identical center in the varunid shore crab, Hemigrapsus nudus . Other studies carried out by the same authors (Thoen, Sayre, Marshall, & Strausfeld, ; Thoen, Marshall, Wolff, & Strausfeld, ; Thoen, Strausfeld, & Marshall, ) show the stomatopods to have elaborate optic lobes and central complex neuropils, most likely due to the high processing demands of their visual system, which has been shown to detect 12 different color channels as well as both linearly and circularly polarized light (Chiou et al, ; Cronin & Marshall, ; Marshall, ; Marshall, Cronin, & Kleinlogel, ).…”

“…Of special note are the large ovoid territories delineated by anti-GAD immunohistology (Figure 2d). These correspond to systems of syn- Thoen, et al, 2018). Anti-TH also resolves part of one of the mushroom body columnar lobes (Clm).…”

Mushroom Body Homology and Divergence across Pancrustacea

“…Because stomatopods are unique amongst crustaceans in possessing elaborated optic lobes that serve a multispectral color and polarization photoreceptor system (Thoen et al, 2017a(Thoen et al, , 2018, it could be argued that mushroom-bodies in the mantis shrimp are unique apomorphies that have evolved specifically to serve those modalities. However, Stomatopoda are an outgroup of Eucarida (Euphausiacea + Decapoda) and the status of mushroom bodies as the ancestral ground pattern is supported by corresponding centers in the lateral protocerebrum of later evolving eumalacostracan lineages.…”