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

Abstract

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 MGFmediated escape is glutamatergic. This electrically coupled sensory network may facilitate rapid escape activation by enhancing the amplitude of giant axon depolarization.

It Cuts Both Ways: An Annelid Model System for the Study of Regeneration in the Laboratory and in the Classroom

“…These interconnections are undoubtedly the basis for observed electrotonic coupling between the LGFs and the resultant bilateral synchronization of LGF action potentials during spike propagation ( Drewes, 1984 ). It has also been demonstrated that lumbriculid giant fiber axons are ensheathed by glial cell membranes, resulting in layers of myelin surrounding the axons ( Figure 2G ) ( Günther, 1976 ; Roots and Lane, 1983 ; Purschke, 2015 ; Knowles, 2017 ; Lybrand et al, 2020 ). The presence of myelination on giant fiber axons functions to increase conduction velocity along the length of the giant fibers and thus is thought to be the basis of observed rapid escape reflexes ( Zoran et al, 1988 ; Drewes and Fourtner, 1990 ; Martinez et al, 2008 ).…”

“…These three giant fibers include one medial (MGF) and a pair of lateral giant (LGF) axons ( Figures 2F,G ). Giant axon dye-filling in Lumbriculus demonstrates that these axons are septate in nature; having distinct, segmental divisions separated by a membranous septum ( Lybrand et al, 2020 ), as opposed to being syncytial, where there are no cellular divisions and thus a continuous cytoplasm between cells. Moreover, each segmentally arranged giant axon is connected via gap junctions (i.e., electrically coupled) allowing for uninterrupted through-conduction of nerve impulses along the length of the giant fiber system ( Mulloney, 1970 ; Brink and Ramanan, 1985 ).…”

“…Studies first carried out by electrophysiologists in the late 1970s ( Günther, 1976 ; Drewes et al, 1978 ), demonstrated remarkable recovery of nervous system function. More recent studies demonstrated re-emergence of neuronal activity as early as 24-h post-amputation ( Lybrand and Zoran, 2012 ; Lybrand et al, 2020 ).…”

“…This rapid recovery of function in the regenerating worm fragment highlights the extensive capacity for regeneration and recovery demonstrated by lumbriculid worms. Most recently, patch clamp recordings carried out with regenerating worm fragments, removed from the posterior end of the worm, demonstrated the emergence of medial giant fiber (MGF) post synaptic potentials 24 h post-amputation ( Lybrand et al, 2020 ). These posterior regenerating fragments undergo the most drastic change in axial position, as they become more anteriorly located following the regeneration of a 7–8 segment head ( Martinez et al, 2005 ; Martinez et al, 2006 ).…”

Co‐created in vivo pharmacology practical classes using the novel organism Lumbriculus variegatus

“…19 This may be due to the different nerve fibers responsible for sensing within these two regions; the medial giant fiber is activated following stimulation of the anterior of L. variegatus while stimulation of the posterior will activate the paired lateral giant fibers. 19 When activated, the giant fibers subsequently activate motor neurons and, while the primary neurotransmitter for the medial giant fiber has been proposed to be glutamate, 50 those regulating the lateral giant fibers have not yet been elucidated. The delayed differential effects observed on helical swimming after treatment with mepyramine (Figure 3D) and loratadine (Figure 4D) may be due to the role of histamine signaling within the lateral giant fibers.…”