Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis

Abstract

The neuroarchitecture of Acoela has been at the center of morphological debates. Some authors, using immunochemical tools, suggest that the nervous system in Acoela is organized as a commissural brain that bears little resemblance to the central, ganglionic type brain of other flatworms, and bilaterians in general. Others, who used histological staining on paraffin sections, conclude that it is a compact structure (an endonal brain; e.g., Raikova 2004; von Graff 1891; Delage Arch Zool Exp Gén 4:109-144, 1886). To address this question with modern tools, we have obtained images from serial transmission electron microscopic sections of the entire hatchling of Symsagittifera roscoffensis. In addition, we obtained data from wholemounts of hatchlings labeled with markers for serotonin and tyrosinated tubulin. Our data show that the central nervous system of a juvenile S. roscoffensis consists of an anterior compact brain, formed by a dense, bilobed mass of neuronal cell bodies surrounding a central neuropile. The neuropile flanks the median statocyst and contains several types of neurites, classified according to their types of synaptic vesicles. The neuropile issues three pairs of nerve cords that run at different dorso-ventral positions along the whole length of the body. Neuronal cell bodies flank the cords, and neuromuscular synapses are abundant. The TEM analysis also reveals different classes of peripheral sensory neurons and provides valuable information about the spatial relationships between neurites and other cell types within the brain and nerve cords. We conclude that the acoel S. roscoffensis has a central brain that is comparable in size and architecture to the brain of other (rhabditophoran) flatworms.

Xenacoelomorpha: a case of independent nervous system centralization?

“…As has been shown in previous studies, a high condensation of neural bodies and their processes characterizes the NS of S. roscoffensis. Confocal and electron microscopic studies have confirmed that, in juveniles, this neural mass fills most of the anterior third of the body (figure 1 and [50]). The so-called brain consists of a compact bilobed mass with a peripheral layer of neuronal cell bodies surrounding a central neuropile, all located around the statocyst, with two ocelli located laterally [50].…”

“…Confocal and electron microscopic studies have confirmed that, in juveniles, this neural mass fills most of the anterior third of the body (figure 1 and [50]). The so-called brain consists of a compact bilobed mass with a peripheral layer of neuronal cell bodies surrounding a central neuropile, all located around the statocyst, with two ocelli located laterally [50]. The NS contains also three pairs of neurite bundles that run along the major body axis: a dorsomedial pair (dmn), a dorsolateral pair (dln) and a ventrolateral pair (vln), all connected by numerous commissures that are arranged irregularly (figure 2c-e; fig.…”

“…The NS contains also three pairs of neurite bundles that run along the major body axis: a dorsomedial pair (dmn), a dorsolateral pair (dln) and a ventrolateral pair (vln), all connected by numerous commissures that are arranged irregularly (figure 2c-e; fig. 2 in [29]) [50,51]. This compact (centralized) arrangement is preserved from the juvenile to the adult stages.…”

“…In fact, the acoel NS is characterized by its high plasticity, which is evident in the very different neuronal arrangements that the acoel species show. A quick comparison of, for instance, acoels belonging to the most basal family (Diopisthoporidae) and those of the most divergent families within the class Crucimusculata reveals very striking differences in neural system arrangement [4,6,[48][49][50][51]. Using the knowledge obtained from several studies, old and new, we are in a position to understand, for the first time, the evolution of the NS within this group (see also [6]), always in accordance with the latest available phylogeny of the Acoela [48].…”

“…In the species of this clade, the NS becomes structurally more complex, forming a compact anterior bilobed brain with a cellular cortex and a dense central neuropile [6,29,50]. This anterior neuronal mass gives rise to a variable number of neurite bundles, which tend to be highly interconnected [6,24,29,50,51]. Over the last decade, several research groups, including ours, have studied some specific species belonging to Crucimusculata, such as Isodiametra pulchra and Symsagittifera roscoffensis, with the NS as their major research objective ( fig.…”