Central circuitry in the jellyfishAglantha digitaleIV. Pathways coordinating feeding behaviour

Abstract

SUMMARYThe hydromedusan jellyfish Aglantha digitale feeds on small planktonic organisms carried to the margin by tentacle flexions. During feeding, the manubrium bends across (`points') and seizes the prey with flared lips. In immobilized preparations, pointing to a source of electrical stimulation was accurate, 70% of the time, to within 15°. Cutting experiments showed that the conduction pathways concerned with pointing and lip flaring are located in eight radial strands consisting of a radial canal,a giant nerve axon and a bundle of small axons with FMRFamide-like immunoreactivity.Application of food juices to sites on the margin and tentacles evoked trains of impulses in the axon bundles (F events; conduction velocity 15.5±3.7 cm s-1) and in the epithelium lining the radial canals (E events; conduction velocity 28.5±3.5 cm s-1). Impulses were conducted circularly in the outer nerve ring (F events) or in the ring canal (E events).Unilateral flexions of the manubrium during pointing arise from preferential excitation of one or more of eight longitudinal `muscle bands' in the wall of the manubrium and peduncle. Lip flaring represents symmetrical contraction of all eight bands. Cutting experiments revealed that F events mediate pointing; E events mediate lip flaring. Thus the endodermal radial canals, which in other hydromedusae mediate protective `crumpling', provide the conduction pathway for manubrial lip flaring. Aglantha's alternative protective response – escape swimming – makes crumpling unnecessary, releasing the pathway for use in feeding.Trains of E events, generated in the manubrium during ingestion, propagate to the margin and inhibit rhythmic (slow) swimming with a duration that depended on their number and frequency. Inhibition of swimming appeared to facilitate transfer of food from the margin to the mouth, but how it comes about is unclear.

The neuroendocrine system of invertebrates: a developmental and evolutionary perspective

“…For example, FMRFamide-expressing cells, mostly bipolar sensory neuron, are concentrated in the tentacles of Aglantha. These neurons control the feeding response: tentacular movement leading to prey capture and ingestion (Mackie et al 2003). FMRFamidergic neurons in the planula larvae of the anthozoan (coral) Hydractinia echinata exert a tonic effect on motility (Katsukura et al 2004).…”

Electrogenesis in the lower Metazoa and implications for neuronal integration

“…at a point where a small axon bundle joins the margin, the manubrium 'pointed' to the stimulation site. Such pointing was found to be accurate to within 15 deg, 70% of the time (Mackie et al, 2003). It was just as accurate when the stimulating electrode was moved to an intermediate position between radial canals as if the radial pathways were linked by circular pathways within the nerve ring (shown as a horizontal cylinder, F, in Fig.…”

“…These axons are shown as part of the 'F' system in Fig. 5; they run down the bell towards the margin alongside each radial canal (Mackie et al, 2003). When Aglantha preparations were stimulated on the outer nerve ring at the base of one of the radial canals, i.e.…”

“…Fig. 6B is a schematic diagram to show the relationships between these different systems (Spencer and Arkett, 1984).Many hydromedusae stop swimming while they are feeding (Horridge, 1955b) and Aglantha is no exception (Mackie et al, 2003). Swimming was inhibited when food was presented directly to the lips or following electrical stimulation of the manubrium; the period of inhibition depended on the stimulus duration.…”

“…The piggyback effect is described in Mackie and Meech (Mackie and Meech, 1995a). The pathways include: (1) the flexion system (F) that mediates the pointing movements seen during feeding (Mackie et al, 2003); (2) the endodermal system (E) that mediates lip flaring and swimming inhibition (Mackie et al, 2012); (3) the swim pacemaker system (P) (Mackie and Meech, 2000); (4) the exumbrellar conduction system (EX) which also inhibits swimming (Mackie and Singla, 1997); the cells in this epithelial pathway are coupled by gap junctions; conduction is unpolarized so that impulses spread in all directions; (5) the ring giant axon (RG) excited by vibration receptors at the bell margin mediates escape swimming via the carrier (C) system and the motor giant axon (MG) (Mackie and Meech, 1995a;Mackie and Meech, 1995b); (6) the nitric oxide pathway (NO) (Moroz et al, 2004); (7) the relay system (R) (Mackie and Meech, 1995a); (8) tentacle nerves include those nerves that feed into the F system (TF), the tentacle giant axon (TG) and the slow tentacle system (TS) (see Mackie and Meech, 1995a;Meech, 1995b, Mackie andMeech, 2000).The Journal of Experimental Biology 542 plexus located in the endodermal walls of the stomach and radial and ring canals (Mackie and Meech, 2008). Neurites belonging to this E system run around the margin adjacent to the inner nerve ring, where the pacemaker neurons are located but direct synaptic contact has yet to be demonstrated anatomically (Mackie et al, 2003).…”