Atlas of the neuromuscular system in the Trachymedusa Aglantha digitale: Insights from the advanced hydrozoan

Abstract

Cnidaria is the sister taxon to bilaterian animals, and therefore, represents a key reference lineage to understand early origins and evolution of the neural systems. The hydromedusa Aglantha digitale is arguably the best electrophysiologically studied jellyfish because of its system of giant axons and unique fast swimming/escape behaviors. Here, using a combination of scanning electron microscopy and immunohistochemistry together with phalloidin labeling, we systematically characterize both neural and muscular systems in Aglantha, summarizing and expanding further the previous knowledge on the microscopic neuroanatomy of this crucial reference species. We found that the majority, if not all (~2,500) neurons, that are labeled by FMRFamide antibody are different from those revealed by anti‐α‐tubulin immunostaining, making these two neuronal markers complementary to each other and, therefore, expanding the diversity of neural elements in Aglantha with two distinct neural subsystems. Our data uncovered the complex organization of neural networks forming a functional “annulus‐type” central nervous system with three subsets of giant axons, dozen subtypes of neurons, muscles, and a variety of receptors fully integrated with epithelial conductive pathways supporting swimming, escape and feeding behaviors. The observed unique adaptations within the Aglantha lineage (including giant axons innervating striated muscles) strongly support an extensive and wide‐spread parallel evolution of integrative and effector systems across Metazoa.

Cytoskeletal and synaptic polarity of LWamide-like+ ganglion neurons in the sea anemone Nematostella vectensis

“…We chose this cell type for initial analysis because its low density facilitates analysis of single cells in live animals and the LWamide-like peptide is expressed in only three of the 32 potential neuronal cell types identified by whole organism transcriptional profiling (Sebe-Pedros et al, 2018), indicating that they represent a relatively homogenous population of neurons. Furthermore, anatomically similar ganglion neurons have been observed in diverse medusozoans (Anderson, 1985;Dupre and Yuste, 2017;Norekian and Moroz, 2020) and LWamidelike peptide precursors are found in diverse cnidarians (Gajewski et al, 1996;Mitgutsch et al, 1999;Nielsen et al, 2019;Plickert et al, 2003), suggesting that they could represent a conserved type of cnidarian neuron. We find that all neurites of LWamide-like+ ganglion neurons have axon-like microtubule polarity but lack plasma membrane diffusion barriers and appear to connect at least in part via bidirectional chemical synapses.…”

Neural versus alternative integrative systems: molecular insights into origins of neurotransmitters

“…To the best of our knowledge, there is only one documented case in Cnidaria, when non-neuronal functions of NO, as a transmitter and an integrator of behaviours, have been 'delegated' to neurons. It was discovered in the trachymedusa Aglantha digitale-a highly advanced hydrozoan with giant axons and annulus type of the central nervous system [162,163]. At least 14 functional conductive systems have been physiologically identified in Aglantha including endodermal and ectodermal epithelial pathways [163][164][165][166][167]-an amazing example of neuroid complexity within a 'simple' jellyfish!…”

Phylogenetics of swimming behaviour in Medusozoa: the role of giant axons and their possible evolutionary origin

“…Also shown is one of a number of ring neurones (RN); position of tentacle slow axons shown by dashed line (modified from Bickell-Page and Mackie, 1991 ; reproduced with permission from the Royal Society, UK). (i) Proximal neurites (arrows) of tentacle giant neurons may make contact with the ring giant axon (RGA)/carrier system in the nerve ring (NR); α-tubulin immunoreactivity (green); scale bar, 30 µm (from Norekian and Moroz, 2020 ; reproduced with permission from John Wiley & Sons). (ii) Processes arising in the region of the ring neurons travel distally (arrows).…”