Novel peripheral motor neurons in the posterior tentacles of the snail responsible for local tentacle movements

Abstract

Three flexor muscles of the posterior tentacles of the snail Helix pomatia have recently been described. Here we identify their local motor neurons by following the retrograde transport of neurobiotin injected into these muscles. The mostly unipolar motor neurons (15-35 µm) are confined to the tentacle digits and send motor axons to the M2 and M3 muscles. Electron microscopy revealed small dark neurons (5-7 µm diameter) and light neurons with 12-18 µm (T1 type) and 18-30 µm diameters (T2 type) in the digits. The diameters of the neurobiotin labeled neurons corresponded to the T1 type light neurons.The neuronal processes of T1 type motor neurons arborize extensively in the neuropil area of the digits and receive synaptic inputs from local neuronal elements involved in peripheral olfactory information processing. These findings support the existence of a peripheral stimulus-response pathway, consisting of olfactory stimulus -local motor neuron -motor response components, to generate local lateral movements of the tentacle tip ("quiver"). In addition, physiological results showed that each flexor muscle receives distinct central motor commands via different peritentacular nerves, and common central motor commands via tentacle digits, respectively. The distal axonal segments of the common pathway can receive inputs from local interneurons in the digits modulating the motor axon activity peripherally without soma excitation. These elements constitute a local microcircuit consisting of olfactory stimulus -distal segments of central motor axons -motor response components, to induce patterned contraction movements of the tentacle. The two local microcircuits described above provide a comprehensive neuroanatomical basis of tentacle movements without the involvement of the CNS.

Anatomical and physiological background permitting spatial odor sensation in stylommatophoran molluscs

“…FMs receive rich innervation by axons of cerebral neurons branching extensively along the muscle fibers and making contacts typical for molluscs [29]. Using anterograde neurobiotin tracing we have demonstrated that FMs received nerve fibers via the olfactory (o.n.)…”

“…For example, the upright position is generated by contraction of the FM3 alone, while upright lateral movement is due to the synchronous contraction of the FM2 and FM3. Contraction of the FM2 and relaxation of the FM3 elicit downward position of tentacles, whereas the horizontal position is generated by the contraction of FM1 and FM2 [29,31]. In summary, it is presumed that FMs are necessary and sufficient to perform all the tentacle movements around the basal pivot.…”

“…The presence of peripheral motor neurons, however, was hypothesized because it was observed that lateral flexion or quiver could be induced in isolated tentacle preparation as well [77]. Recently we have described neurons in the digits, neurites of which innervate muscle fibers both in flexor and tegumental muscles [29]. In order to reveal neuronal elements innervating FMs, neurobiotin tracing was performed via the tentacle FMs.…”

“…Consequently, the muscles capable of eliciting quiver are FM2 and FM3. Based on these neuroanatomical results, it was supposed that part of the population of light type neurons of digits fulfill motor neuron function in the ventral and lateral digits [29].…”