Dissecting a neuron network: FIB-SEM-based 3D-reconstruction of the visual neuropils in the sea spider Achelia langi (Dohrn, 1881) (Pycnogonida)

Abstract

BackgroundThe research field of connectomics arose just recently with the development of new three-dimensional-electron microscopy (EM) techniques and increasing computing power. So far, only a few model species (for example, mouse, the nematode Caenorhabditis elegans, and the fruit fly Drosophila melanogaster) have been studied using this approach. Here, we present a first attempt to expand this circle to include pycnogonids, which hold a key position for the understanding of arthropod evolution. The visual neuropils in Achelia langi are studied using a focused ion beam-scanning electron microscope (FIB-SEM) crossbeam-workstation, and a three-dimensional serial reconstruction of the connectome is presented.ResultsThe two eyes of each hemisphere of the sea spider’s eye tubercle are connected to a first and a second visual neuropil. The first visual neuropil is subdivided in two hemineuropils, each responsible for one eye and stratified into three layers. Six different neuron types postsynaptic to the retinula (R-cells) axons are characterized by their morphology: five types of descending unipolar neurons and one type of ascending neurons. These cell types are also identified by Golgi impregnations. Mapping of all identifiable chemical synapses indicates that the descending unipolar neurons are postsynaptic to the R-cells and, hence, are second-order neurons. The ascending neurons are predominantly presynaptic and sometimes postsynaptic to the R-cells and may play a feedback role.ConclusionsComparing these results with the compound eye visual system of crustaceans and insects – the only arthropod visual system studied so far in such detail – we found striking similarities in the morphology and synaptic organization of the different neuron types. Hence, the visual system of pycnogonids shows features of both chelicerate median and mandibulate lateral eyes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-014-0059-3) contains supplementary material, which is available to authorized users.

Techniques and applications of three‐dimensional electron microscopy in entomological research

“…melanogaster , the detailed structure of the compound eye visual system in sea spider, Achelia langi , were studied through FIB‐SEM based 3D reconstruction (Lehmann et al . ). These revolutionary serial section 3DEM techniques make it possible to construct 3D structures of large volumes of tissue (hundreds of micrometers), and it is sure to overcome the limitations of structural studies using 2D images.…”

The Diversity of Spine Synapses in Animals

“…In the sea spider (Pycnogonida: another chelicerate group), Achelia langi , a single presynaptic terminal can contact five small postsynaptic processes. While some of the postsynaptic processes can look rather spine-like in profile, three-dimensional serial reconstructions of postsynaptic processes indicate that synapses occur mainly along the processes, and no definitive postsynaptic spines are described (Lehmann et al 2014). …”

Sense organs in Pycnogonida: A review

“…The eyes of a few sea spiders have indeed been studied in some detail, and from this small body of knowledge, we can assume that the above‐described R‐cell structure and the wiring of their axons probably holds true for Pycnogonida as well (e.g., Heß, Melzer, and Smola (); Jarvis and King (); Morgan (); Sokolow (); Wiren ()). The trajectories of R‐cell axons and the visual neuropils have recently been studied by Lehmann, Heß, and Melzer () and Lehmann, Heß, Wanner, and Melzer ().…”

“…In the present report, we have therefore not only summarized published knowledge, but also present original data from, for example, ultrathin sections we collected in the past two decades as by‐products of our studies on pycnogonid eyes (Heß et al., ; Lehmann et al., ; Lehmann, Heß, Wanner, et al. ) and glands (Melzer, Heβ, Dunkel, Ludwig, & Smola, ).…”