Back to the Basics: Cnidarians Start to Fire

Abstract

The nervous systems of cnidarians, pre-bilaterian animals that diverged close to the base of the metazoan radiation, are structurally simple and thus have great potential to reveal fundamental principles of neural circuits. Unfortunately, cnidarians have thus far been relatively intractable to electrophysiological and genetic techniques and consequently have been largely passed over by neurobiologists. However, recent advances in molecular and imaging methods are fueling a renaissance of interest in and research into cnidarians nervous systems. Here, we review current knowledge on the nervous systems of cnidarian species and propose that researchers should seize this opportunity and undertake the study of members of this phylum as strategic experimental systems with great basic and translational relevance for neuroscience.

Keywords: BRAIN Initiative; CRISPR; Hydra; Nematostella; imaging.

Figure 1. Cnidarians as model organisms for studies of nervous systems

A: Schematic phylogenetic tree showing the relationships of the five classes within the phylum Cnidaria. Species of cnidarians used for research on nerve systems and referred to in this Review are listed. Complete genome sequences are available for several cnidarian species (marked with asterisk) [21]. B: Schematic phylogenetic tree showing main branches of metazoan evolution and position of Cnidaria among the non-bilaterian Metazoa. As the phylogenetic position of comb-jellies (Ctenophora) remains controversial [– 15], the branch leading to this group is represented by a dashed line.

Figure 2. Distinctive features of cnidarian nervous system

A diffuse nerve net is a basic design of cnidarian nerve systems. Nerve net of the sea anemone Nematostella vectensis revealed by expression of a mCherry protein under nerve-specific elav promotor. Modified from [98]. Local condensation of the nerve net is observed in most cnidarians [69,121,122]. For instance, in Hydra high density of the JRI-positive sensory neurons is observed around the mouth opening (hypostome) of a polyp. Modified from [93]. Chemical heterogeneity of the cnidarian nerve net contrasts its apparent morphological simplicity. A broad range of neurotransmitters present in cnidarian nerve cells are expressed by particular subsets of neurons. For instance, in Hydra RFamide (left) and GLWamide (right) are produced by two apparently not-overlapping populations of neurons. Modified from [93]. Sensory cnidocytes represent a type of mechanosensory cell found exclusively in cnidarians. Mechanical stimulation of a resting cnidocyte (left) triggers rapid discharge of a nematocyst and release of a harpoon to spear and paralyze prey. Modified from [123]. Complex sense organs are found in cnidarians. A statocyst from the umbellar margin of the hydrozoan jellyfish Aglantha contains a concretion (c) surrounded by sensory cells (sc) with sensory cilia (sh), that are connected to the umbrella’s outer nerve ring (onr). Declination of the concretion stimulates cilia, enabling the medusa’s vestibular sense. Modified from [66]. Bidirectional synapses are common for cnidarian. An electron micrograph of a synapse between two axons in the scyphozoan Cyanea represents neurotubules (t) and small vesicles (bs) on both sides of a synaptic cleft (s). Modified from [36]. Plasticity and regeneration are characteristic for nervous systems of cnidarians undergoing constant asexual proliferation. In vivo imaging of transgenic cells (here a ganglion neuron of Hydra, modified from [124]) allows studying how this plasticity is accomplished by integrating stem cell derived migratory neuronal precursor cells into the nervous system. Complex behaviours, such as somersaulting in Hydra, emerge from the activity of simple nerve nets; the cellular and molecular processes behind remain poorly understood. Modified from [92].