Coupled sensory interneurons mediate escape neural circuit processing in an aquatic annelid worm, Lumbriculus variegatus

• Published in: Journal of comparative neurology (1911) Vol. 528; no. 3; pp. 468 - 480
• Main Authors: Lybrand, Zane R., Martinez‐Acosta, Veronica G., Zoran, Mark J.
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 15-02-2020; Wiley Subscription Services, Inc
• Subjects: annelid; Body wall; Conduction; couple network; Dendrites; Depolarization; Electrical stimuli; electrical synapse; Escape behavior; giant interneuron; Glutamatergic transmission; Glutamic acid receptors; Immunoreactivity; Information processing; Interneurons; Lumbriculus variegatus; RRID:AB_141357; RRID:AB_141596; RRID:AB_1500929; RRID:AB_1566261; RRID:AB_396353; RRID:AB_880229; Sensory integration; Sensory neurons; sensory processing; silent synapse; giant interneuron; sensory processing; RRID:AB_1566261; couple network; RRID:AB_141357; RRID:AB_1500929; silent synapse; annelid; RRID:AB_880229; electrical synapse; RRID:AB_141596; RRID:AB_396353
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.24769

The interneurons associated with rapid escape circuits are adapted for fast pathway activation and rapid conduction. An essential aspect of fast activation is the processing of sensory information with limited delays. Although aquatic annelid worms have some of the fastest escape responses in nature, the sensory networks that mediate their escape behavior are not well defined. Here, we demonstrate that the escape circuit of the mud worm, Lumbriculus variegatus, is a segmentally arranged network of sensory interneurons electrically coupled to the central medial giant fiber (MGF), the command‐like interneuron for head withdrawal. Electrical stimulation of the body wall evoked fast, short‐duration spikelets in the MGF, which we suggest are the product of intermediate giant fiber activation coupled to MGF collateral dendrites. Since these contact sites have immunoreactivity with a glutamate receptor antibody, and the glutamate receptor antagonist 6‐cyano‐7‐nitroquinoxaline‐2,3‐dion abolishes evoked MGF responses, we conclude that the afferent pathway for MGF‐mediated escape is glutamatergic. This electrically coupled sensory network may facilitate rapid escape activation by enhancing the amplitude of giant axon depolarization.
The giant interneuron (magenta) for rapid escape in the mud worm, Lumbriculus variegatus, is activated by sensory interneuron inputs (green) to its collateral dendrites. These sites of electrical coupling from sensory interneurons to the giant interneuron collaterals (blue) and generate spikelets in the giant interneuron (green recording), which we suggest sum with postsynaptic potentials (blue recording) and regulate sensory processing by priming giant axon spiking (magenta recording).