Central Neural Circuitry in the Jellyfish <i>Aglantha</i>

Abstract

Like other hydrozoan medusae, Aglantha lacks a brain, but the two marginal nerve rings function together as a central nervous system. Twelve neuronal and two excitable epithelial conduction systems are described and their interactions summarized. Aglantha differs from most medusae in having giant axons. It can swim and contract its tentacles in two distinct ways (escape and slow). Escape responses are mediated primarily by giant axons but conventional interneurons are also involved in transmission of information within the nerve rings during one form of escape behavior. Surprisingly, giant axons provide the motor pathway to the swim muscles in both escape and slow swimming. This is possible because these axons can conduct calcium spikes as well as sodium spikes and do so on an either/or basis without overlap. The synaptic and ionic bases for these responses are reviewed. During feeding, the manubrium performs highly accurate flexions to points at the margin. At the same time, the oral lips flare open. The directional flexions are conducted by FMRFamide immunoreactive nerves, the lip flaring by an excitable epithelium lining the radial canals. Inhibition of swimming during feeding is due to impulses propagated centrifugally in the same epithelium. Aglantha probably evolved from an ancestor possessing a relatively simple wiring plan, as seen in other hydromedusae. Acquisition of giant axons resulted in considerable modification of this basic plan, and required novel solutions to the problems of integrating escape with non-escape circuitry.

The evolution of nervous system centralization

“…For example, some cnidarian medusae possess an elaborate nerve ring around their central opening (manubrium) in addition to their diffuse nerve net (Mackie 2004). This nerve ring reflects a considerable degree of centralization.…”

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

“…This is seen in the separation of the two diffuse networks of the subumbrella of scyphomedusae -the 'giant fiber nerve net' and the 'diffuse nerve net' (see Satterlie and Eichinger, 2014). Similarly, separate motor and sensory networks are found in the nerve rings of hydromedusae (Arkett and Spencer, 1986a;Arkett and Spencer, 1986b;Mackie et al, 2003;Mackie, 2004), and in four species representing three hydrozoan orders, sensory cells were components of all FMRFamideimmunoreactive nerve nets while immunoreactivity was absent in known motor networks (Mackie et al, 1985). Further examination of the FMRFamide-immunoreactive nets of Polyorchis indicated that, in addition to inclusion of sensory cells, the networks were frequently associated with smooth muscle bands for fields, but not the striated musculature used in swimming (Grimmelikhuijzen and Spencer, 1984;Spencer, 1988), raising the possibility that the FMRFamide networks are mixed sensory-motor nets.…”

“…Similar integrative interactions occur between the largely parallel conducting systems of the inner and outer nerve rings of hydromedusae. Here, the number of distinct conducting systems can be considerable, as shown in the hydromedusa Aglantha digitale (Mackie, 2004).…”

“…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.…”

Origin and early evolution of neural circuits for the control of ciliary locomotion

“…In these circuits, motoneurons form a network connected by gap junctions, allowing the spread of currents to large motor areas. These networks are controlled by fast giant axons, such as in the hydrozoan Aglantha [67], that receive input from mechanosensory cells.…”