Bilaterally symmetrical rhopalial nervous system of the box jellyfish Tripedalia cystophora

Abstract

Cubomedusae, or box jellyfish, have the most elaborate visual system of all cnidarians. They have 24 eyes of four morphological types, distributed on four sensory structures called rhopalia. Box jellyfish also display complex, probably visually guided behaviors such as obstacle avoidance and fast directional swimming. Here we describe the strikingly complex and partially bilaterally symmetrical nervous system found in each rhopalium of the box jellyfish, Tripedalia cystophora, and present the rhopalial neuroanatomy in an atlas-like series of drawings. Discrete populations of neurons and commissures connecting the left and the right side along with two populations of nonneuronal cells were visualized using several different histochemical staining techniques and electron microscopy. The number of rhopalial nerve cells and their overall arrangement indicates that visual processing and integration at least partly happen within the rhopalia. The larger of the two nonneuronal cell populations comprises approximately 2,000 likely undifferentiated cells and may support a rapid cell turnover in the rhopalial nervous system.

Do jellyfish have central nervous systems?

“…In all anatomical respects, these latter structures give the rhopalia the look of ganglia found in bilateral animals (Fig.10). As a testament to the integrative capabilities of the rhopalia, the various types of eyes have bilateral, directional neuronal tracts that run between the eyes and the pacemaker neuropil, and commissures connecting the tracts (Parkefelt et al, 2005;Garm et al, 2006;Skogh et al, 2006). Both bidirectional and unidirectional synapses have been found in the retinal and pacemaker regions (Gray et al, 2009).…”

“…Even the compressed networks are just that -net-like groups of neurons that serve particular functions. The cubomedusan ganglia (the rhopalia) include both compressed networks and distinct neuronal tracts and commissures (Parkefelt et al, 2005;Garm et al, 2006;Skogh et al, 2006), suggesting a development of integrating centers that goes beyond the concept of nerve net compression and showing a bilateral anatomy that bucks the organization trend of radial symmetry. But regardless of how we want to label the condensation of nervous tissue in jellyfish, one common feature brings it in parallel with bilateral central nervous systems -the close association between this condensation and the elaboration of sensory structures, some of which are diffusely arranged in marginal structures including tentacles, and some of which are placed in more widely spaced structures around the bell.…”

Pattern and contrast dependent visual response in the box jellyfish Tripedalia cystophora

“…Electrophysiological experiments and morphological examinations indicate that the visual processing mostly takes place in the rhopalial nervous systems (Satterlie and Nolen, 2001;Parkefelt et al, 2005;Garm and Mori, 2009;Parkefelt and Ekström, 2009). In the adult medusa, only approximately 1000 neurons are found here besides the photoreceptors (Skogh et al, 2006). This limited number of neurons has to process spatial information from at least the two lens eyes and possibly also the slit eyes.…”

“…The possible image formation in the slit eyes, seeing the world in horizontal bands, is intriguing and still awaits proof from behavioural experiments. Cnidarians are often accused of being brainless (Wehner, 2005), but there is no doubt that at least hydromedusae and cubomedusae possess a CNS (Passano, 1976;Mackie, 2004;Skogh et al, 2006;Garm et al, 2007c). In cubomedusae, the CNS is composed of four parallel rhopalial nervous systems interconnected by a ring nerve (Satterlie, 2002;Garm et al, 2007c;Satterlie, 2011).…”

The search for ancestral nervous systems: an integrative and comparative approach

“…Once again, areas of interaction between these different nerve nets will represent sites of neuronal integration representative of Horridge's 'central properties', where emergent properties of the nervous system will go well beyond those of the individual contributing nerve nets. These interactions are carried to the extreme (for cnidarians) in those species that have more centralized nervous components, including the ganglion-like rhopalia or nerve rings composed of multiple, compressed nerve networks (Mackie, 2004;Parkefelt et al, 2005;Garm et al, 2006;Skogh et al, 2006;Satterlie, 2011. Several organizational concepts are suggested for the evolution of nervous systems in basal organisms and their ancestors that go well beyond the singular diffuse nerve net concept.…”