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

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...

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Bibliographic Details
Published in:Journal of comparative neurology (1911) 2020-02, Vol.528 (3), p.468-480
Main Authors: Lybrand, Zane R., Martinez‐Acosta, Veronica G., Zoran, Mark J.
Format: Article
Language:English
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
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Summary: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).
ISSN:0021-9967
1096-9861
DOI:10.1002/cne.24769