The catecholaminergic nerve plexus of Holothuroidea

Abstract

Catecholamines have been extensively reported to be present in most animal groups, including members of Echinodermata. In this study, we investigated the presence and distribution of catecholaminergic nerves in two members of the Holothuroidea, Holothuria glaberrima (Selenka, 1867) (Aspidochirotida, Holothuroidea) and Holothuria mexicana (Ludwig, 1875) (Aspidochirotida, Holothuroidea), by using induced fluorescence for catecholamines on tissue sections and immunohistochemistry with an antibody that recognizes tyrosine hydroxylase. The presence of a catecholaminergic nerve plexus similar in distribution and extension to those previously reported in other members of Echinodermata was observed. This plexus, composed of cells and fibers, is found in the ectoneural component of the echinoderm nervous system and is continuous with the circumoral nerve ring and the radial nerves, tentacular nerves, and esophageal plexus. In addition, fluorescent nerves in the tube feet are continuous with the catecholaminergic components of the radial nerve cords. This is the first comprehensive report on the presence and distribution of catecholamines in the nervous system of Holothuroidea. The continuity and distribution of the catecholaminergic plexus strengthen the notion that the catecholaminergic cells are interneurons, since these do not form part of the known sensory or motor circuits and the fluorescence is confined to organized nervous tissue.

Novel markers identify nervous system components of the holothurian nervous system

“…However, some of the differences observed in the enteric nervous system of the three species could also be due to variations associated with the level of the intestinal tissue that was studied and not necessarily species differences. Such differences have been well documented in H. glaberrima where, for example an intestinal catecholaminergic plexus is observed in the esophagus and descending small intestine but is not found in other intestinal regions (Diaz-Balzac et al 2010b). In this respect, it is important to highlight that the posterior (large) intestine of H. mexicana was studied, but for the other two species the sections were obtained at mid-body level, thus it is not clear if the intestinal tissue at that level corresponds (anatomically or functionally) to a more small intestine (nutrient absorptive function) or large intestine (feces compaction function) type.…”

“…Similarly, anti-nurr1 is the first marker that appears to preferentially identify cells of the hyponeural component over those of the ectoneural component, contrary to anti-galanin, which preferentially identify cells and fibers of the ectoneural component (Diaz-Miranda et al 1996). This is particularly surprising in view of the fact that in vertebrates, Nurr1 function has been associated with the catecholaminergic neurotransmitter system (Zetterstrom et al 1997), but previous studies from our group have shown that the holothurian catecholaminergic system is present within the ectoneural component of the radial nerve cord (Diaz-Balzac et al 2010b). Finally, most of the cells immunoreactive to anti-PH3 and anti-pax6 were found outside of the radial nerve cord, suggesting that they correspond to a peripheral nervous system component and that most of the fibers identified by these antibodies within the radial nerve cord itself might correspond to afferent fibers originating from the somas localized in peripheral regions, such as the podial nerve or enteric nervous system.…”

“…1A–B). The nervous system in these organs has been thoroughly described in previous studies by our group (Diaz-Balzac et al 2010a; Diaz-Balzac et al 2010b; Diaz-Balzac et al 2007; Diaz-Miranda et al 1995; Diaz-Miranda et al 1996) and thus provides an excellent starting point for comparison of the immunoreactivity observed with the new markers.…”

Holothurian Nervous System Diversity Revealed by Neuroanatomical Analysis

“…Smaller subpopulations of neurons have also been characterized by using previously described nervous system markers, particularly neurotransmitters or their synthesizing enzymes or neuropeptides. Thus, the gabaergic and catecholaminergic nervous system components of echinoderms have been described [ 9 , 10 ] as have been many neurons, neuroendocrine cells and fibers that express neuropeptides. This is the case for SALMFamide [ 11 , 12 ], GFSKLYFamide [ 13 ], galanin [ 14 ], and FMRFamide [ 15 ].…”

Localization and distribution of nitric oxide synthase and other neuronal markers in the podia of Holothuria arguinensis

“…Until recently, almost all knowledge of the nervous system of echinoderms was based on classical histology carried out early during the last century and, more recently, on electron microscopy studies (e.g., Bouland et al., 1982; Cavey, 2006; Flammang & Jangoux, 1992; Hyman, 1955; McKenzie, 1987; Pentreath & Cobb, 1972; VandenSpiegel et al., 1995). With the development of new neural markers, neuronal populations expressing different neurotransmitters, such as catecholamines and neuropeptides, have been identified, contributing to a more comprehensive view of the echinoderm nervous system (Díaz‐Balzac, Abreu‐Arbelo, & García‐Arrarás, 2010; Díaz‐Balzac & García‐Arrarás, 2018; Díaz‐Balzac, Mejías, Jiménez, & García‐Arrarás, 2010; Díaz‐Balzac et al., 2007, 2014; Díaz‐Miranda, Blanco, & Garcia‐Arraras, 1995; Hoekstra, Moroz, & Heyland, 2012; Inoue, Tamori, & Motokawa, 2002).…”