Holothurian Nervous System Diversity Revealed by Neuroanatomical Analysis

Abstract

The Echinodermata comprise an interesting branch in the phylogenetic tree of deuterostomes. Their radial symmetry which is reflected in their nervous system anatomy makes them a target of interest in the study of nervous system evolution. Until recently, the study of the echinoderm nervous system has been hindered by a shortage of neuronal markers. However, in recent years several markers of neuronal and fiber subpopulations have been described. These have been used to identify subpopulations of neurons and fibers, but an integrative study of the anatomical relationship of these subpopulations is wanting. We have now used eight commercial antibodies, together with three antibodies produced by our group to provide a comprehensive and integrated description and new details of the echinoderm neuroanatomy using the holothurian Holothuria glaberrima (Selenka, 1867) as our model system. Immunoreactivity of the markers used showed: (1) specific labeling patterns by markers in the radial nerve cords, which suggest the presence of specific nerve tracts in holothurians. (2) Nerves directly innervate most muscle fibers in the longitudinal muscles. (3) Similar to other deuterostomes (mainly vertebrates), their enteric nervous system is composed of a large and diverse repertoire of neurons and fiber phenotypes. Our results provide a first blueprint of the anatomical organization of cells and fibers that form the holothurian neural circuitry, and highlight the fact that the echinoderm nervous system shows unexpected diversity in cell and fiber types and their distribution in both central and peripheral nervous components.

Initial report of γ-aminobutyric acidergic locomotion regulatory system and its 3-mercaptopropionic acid-sensitivity in metamorphic juvenile of sea urchin, Hemicentrotus pulcherrimus

“…The pharmacological response of TF to GABA in major echinoderm species 12,28,29 , and its immunohistochemical detection was reported in starfish 11 and sea cucumber 30 , but not in sea urchins to date. The present striking GABA-IS site was the gaiter region of the juvenile PP.…”

A START-domain-containing protein is a novel marker of nervous system components of the sea cucumber Holothuria glaberrima

“…To tackle this problem, the search and characterization of new markers capable of identifying neurons and plexi that form the echinoderm nervous system components are needed. Our lab and those of others have identified various antibody markers for cells and fibers (Diaz-Miranda et al 1995a,b, 1996, Diaz-Balzac et al 2010, 2012, 2014, 2016). In general, the markers fall into two large categories; the first being those antibodies that recognize what are supposed to be the echinoderm homologs of the antigens recognized by the antibodies in other animal species.…”

“…Here we find antibodies to neurotransmitters such as serotonin (Murabe et al 2008), GABA (Newman and Thorndyke 1994) and histamine (Hoekstra et al 2012) or to their synthesizing enzymes, such as tyrosine hydroxylase (Diaz-Balzac et al 2010). Other antibodies recognize echinoderm peptides (Diaz-Miranda et al 1995), or proteins associated with the nervous system such as synaptotagmin (Burke et al 2006), calbindin (Diaz-Balzac et al 2012) or β-tubulin (Diaz-Balzac et al 2016). The second category are antibodies that label specific components of the nervous system, but whose target antigen is not known.…”

Sea Urchins as an Inspiration for Robotic Designs

“…A variety of neurochemical markers including Pax6, Calbindin, PH3, GABA, GFSKLYFamide, TH, and PH3 identify distinct regions of the endo-and ecto-neural parts of the radial nerve fibers. The radial nerves are composed of distinct sub-systems located in different parts of the sea cucumber body [14]. While the echinoderm central nervous system is not centralized, and rather simple on a gross morphological level, it is nevertheless complex on a neurochemical level.…”

“…While the echinoderm central nervous system is not centralized, and rather simple on a gross morphological level, it is nevertheless complex on a neurochemical level. This neurochemical specialization might be more pronounced in holothurians, with their compressible bodies, than in the rigid-bodied echinoids [14]. The basiepithelial nerve plexus of the sea urchin Centrostephanus longispinus contains strands of nerve fibers measuring between 0.1 and 2.0 µm in diameter, originating from multipolar neurons [15].…”