Two pairs of tentacles and a pair of procerebra: optimized functions and redundant structures in the sensory and central organs involved in olfactory learning of terrestrial pulmonates

Abstract

SummaryTerrestrial pulmonates can learn olfactory-aversion tasks and retain them in their long-term memory. To elucidate the cellular mechanisms underlying learning and memory, researchers have focused on both the peripheral and central components of olfaction: two pairs of tentacles (the superior and inferior tentacles) and a pair of procerebra, respectively. Data from tentacleamputation experiments showed that either pair of tentacles is sufficient for olfactory learning. Results of procerebrum lesion experiments showed that the procerebra are necessary for olfactory learning but that either one of the two procerebra, rather than both, is used for each olfactory learning event. Together, these data suggest that there is a redundancy in the structures of terrestrial pulmonates necessary for olfactory learning. In our commentary we exemplify and discuss functional optimization and structural redundancy in the sensory and central organs involved in olfactory learning and memory in terrestrial pulmonates.

Siphonariid development: Quintessential euthyneuran larva with a mantle fold innovation (Gastropoda; Panpulmonata)

“…The procerebra and cerebral tubes (=cerebral glands) have been identified as synapomorphies of the “Pulmonata” (Haszprunar & Huber, ; Van Mol, , ). Although these structures were at one time described as neurosecretory (Haszprunar & Huber, ), more recent neurophysiological research on terrestrial slugs in the genera Limax and Helix has shown that the procerebra of stylommatophorans are involved in neural processing of olfactory information and in odorant‐based learning (Gelperin & Tank, ; Ermentrout, Wang, & Gelperin, ; others reviewed by Matsuo, Kobayashi, Yamagishi, & Ito, ). Longley () showed that epithelium of the cerebral tubes of Cornu ( Helix) aspersum (O.F.…”

“…Siphonaria denticulata has neither cephalic nor labial tentacles, which provide the olfactory inputs to the procerebra of stylommatophorans such as C. aspersum (Matsuo et al, ). We can only speculate that chemoreceptors distributed throughout peri‐oral epidermis of S. denticulata provide the major sensory input to their procerebra.…”

Anatomical and physiological background permitting spatial odor sensation in stylommatophoran molluscs

“…Terestrial snails and slugs perceive odor molecules by two pairs of tentacles: the longer ones called superior tentacles (ommatophores) which are necessary for food orientation, while the shorter ones (rhinophores) called inferior tentacles and they are necessary for trailing [9,10,66,103]. Superior tentacles are required therefore for long-distance chemoreception and inferior tentacles generally thought to be closerange chemoreceptor organs.…”

Octopaminergic system in the central nervous system of the terrestrial slug Limax

“…The memory can be established by a single pairing of the two stimuli (Sahley et al, 1981). The formation and the retention and/or retrieval of the odoraversion memory critically depend on the structure in the central nervous system (CNS) called the procerebrum (PC), which functions as a higher olfactory center in the terrestrial pulmonates (Gelperin, 1999;Kasai et al, 2006;Watanabe et al, 2008;Matsuo et al, 2011). Oscillatory activity of the local field potential (LFP) recorded on the surface of the PC is considered to reflect the odor information processing by the animal (Gelperin and Tank, 1990).…”