Neural Circuit Mediating Tentacle Withdrawal inHelix aspersa,With Specific Reference to the Competence of the Motor Neuron C3

Abstract

The tentacle withdrawal reflex in the terrestrial snail Helix aspersa involves bending and retraction of the tentacles. When elicited by mechanical stimulation of the tentacle, the reflex is mediated by the conjoint action of the central and peripheral nervous systems. The neural circuit underlying the stimulus-response pathways was studied in vitro using a combination of morphological and physiological techniques. Sensory input caused by stimulation of the nose (situated at the superior tentacle's tip) first passes into the tentacle ganglion. Motor fibers are likely excited in the tentacle ganglion to form a peripheral stimulus-response pathway. While still in the tentacle ganglion, the excitation caused by a brief stimulus is transformed into a prolonged neuronal discharge. This modified signal travels, via the olfactory nerve, to the cerebral ganglion where it excites the giant motor neuron C3 along with numerous smaller motor neurons. Afferent input to C3 also arrives from several other sources. The afferent convergence is followed by a marked divergence of C3's output. C3 innervates the muscles mediating both tentacle retraction and tentacle bending through multiple cerebral nerves. Thus C3's pattern of effector innervation allows this single cell to elicit and coordinate both components of the tentacle withdrawal reflex. Lesion experiments indicate that C3 is responsible for 85% of the central contribution to tentacle retraction, though C3 is actually sufficient to mediate maximal muscle contraction as evidenced by intracellular stimulation. In addition to C3, three groups of putative central motor neurons were identified through nerve backfills and nerve recordings. The additional motor neurons mediating tentacle retraction are important for maximizing the rate of muscle contraction, whereas those mediating tentacle bending are likely more important for nondefensive behaviors. These neurons are arranged in parallel with C3, but unlike C3, each of these neurons innervates only a single effector or portion thereof. Given C3's direct innervation of multiple effectors and its sufficiency to evoke strong responses in those effectors, we conclude that C3 is paramount in eliciting and coordinating tentacle withdrawal.

Phosphorylation by cAMP-dependent protein kinase is essential for synapsin-induced enhancement of neurotransmitter release in invertebrate neurons

“…After digestion, ganglia were repeatedly washed in L15, pinned on a Sylgard-coated plastic dish in L15 and the connective sheaths covering the neurons were removed by fine forceps and scissors. Neurons C1, C3 and B2 (Cottrell, 1977;Prescott et al, 1997) were removed from the ganglia with their initial axonal segment and transferred to plastic culture dishes (Falcon 1008) containing 5% Aplysia hemolymph and 0.01% bovine serum albumin (BSA) in modified L15. Under these conditions, neurons failed to adhere to the plastic substrate and, after 12-48 hours, retracted their neurites, forming spherical somata devoid of processes.…”

Anatomical and physiological background permitting spatial odor sensation in stylommatophoran molluscs

“…Neurons of the g3 and g5 clusters are labeled through Ptns exclusively, therefore it can be suggested that these cells are motoneurons. The functionally and morphologically identified solitary FMRFamidecontaining C3 neuron is labeled via the olfactory and both Pt nerves, and the participation of this cell in the tentacle withdrawal reflex and tentacle graded retraction was described [12,82]. We have observed that the position of neurons labeled via the Acta Biologica Hungarica 67, 2016 olfactory and Pt nerves fall into the areas where neurons are located innervating the head areas.…”

Neuronal background of positioning of the posterior tentacles in the snail Helix pomatia

“…Contrary to the distinct motor pathways, the common pathway via the olfactory nerve which innervate the tegumental, flexor and retractor muscles is probably responsible for the withdrawal reflex and the graded shortening of the tentacles when all muscles of the tentacle are contracted (Prescott et al 1997, for rev. Chase 2002.…”

“…Only a solitary labeled neuron the MtC3 cell was identified functionally, taking part both in the tentacle withdrawal reflex and the graded tentacle retraction (Cottrell et al 1983, Chase and Hall 1996, Prescott et al 1997, Nikitin et al 2005. Therefore it is difficult to render exact function (sensory, motor or modulator) to any group of the labeled neurons.…”

“…Consequently it can easily be distinguished from other tentacle movements, such as tentacle withdrawal (Prescott et al 1997, for rev. Chase 2002 and local movements of the tentacle tip (Lemair and Chase 1998, Nikitin et al 2005, 2008.…”