Unilateral memory storage in the procerebrum of the terrestrial slug Limax

Matsuo, Ryota; Kawaguchi, Eri; Yamagishi, Miki; Amano, Tsuyoshi; Ito, Etsuro

doi:10.1016/j.nlm.2009.11.008

Cited by 25 publications

(19 citation statements)

References 20 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In terrestrial slug Limax it was inferred from unilateral ablation experiments that the odor-aversion memory stored unilaterally in one side of the procerebrum and that the storage side is randomly determined (Matsuo et al, 2010). This paper showed that the unilateral storage of the memory is equally distributed in the population, meaning a 50% chance to impair the memory by random inactivation.…”

Section: Discussionmentioning

confidence: 86%

Taste Familiarity Is Inversely Correlated with Arc/Arg3.1 Hemispheric Lateralization

Inberg

Elkobi

Edri

et al. 2013

Journal of Neuroscience

View full text Add to dashboard Cite

Biochemical, electrophysiological, and imaging studies suggest that the anterior part of the insular cortex (IC) serves as primary taste cortex, whereas fMRI studies in human propose that the anterior IC is also involved in processing of general novelty or saliency information. Here, we compared activity regulated cytoskeleton associated protein (Arc)/Arg3.1 protein levels in the rat IC following administration of familiar versus novel tastes. Surprisingly, there was no correlation between novel taste and Arc/Arg3.1 levels when measured as the sum of both left and right insular cortices. However, when left and right IC were examined separately, Arc/Arg3.1 level was lateralized following novel taste learning. Moreover, Arc/Arg3.1 lateralization was inversely correlated with taste familiarity, whereas the high lateralization of Arc/Arg3.1 expression observed following novel taste learning is reduced proportionally to the increment in taste familiarity. In addition, unilateral inhibition of protein synthesis in the IC had asymmetrical effect on memory, inducing strong memory impairment similarly to bilateral inhibition or memory preservation, indicating that hemispheric lateralization is central for processing taste saliency information. These results provide indications, at the gene level of expression, for the role of IC lateralization in processing novel taste information and for the asymmetrical contribution of protein synthesis in each hemisphere during memory consolidation.

show abstract

Section: Discussionmentioning

confidence: 86%

Taste Familiarity Is Inversely Correlated with Arc/Arg3.1 Hemispheric Lateralization

Inberg

Elkobi

Edri

et al. 2013

Journal of Neuroscience

View full text Add to dashboard Cite

show abstract

“…The tentacle amputation of the slugs (12-13 weeks post hatching) was performed under anesthesia, as described previously (Yamagishi et al, 2008;Matsuo et al, 2010b -1 Hepes, pH 7.0) was injected into the body cavity to improve the recovery from anesthetization. After surgery, two to five (usually three) slugs were transferred to a plastic container and maintained with free access to the humidified powder mixture until the next procedure -that is, in vitro LFP recording or histological analysis.…”

Section: Surgerymentioning

confidence: 99%

Effects of tentacle amputation and regeneration on the morphology and activity of the olfactory center of the terrestrial slug Limax valentianus

Matsuo

Kobayashi

Tanaka

et al. 2010

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

SUMMARYThe tentacles of pulmonates regenerate spontaneously following amputation. The regenerated tentacle is equipped with all the elements necessary for normal olfactory functioning, and the slugs can behave as well as they did before the tentacle amputation. However, it is not known what changes occur to the olfactory center procerebrum in the brain at the morphological and physiological levels. Here, we investigated the innervation of tentacular nerves into the procerebrum by examining the size of the terminal mass (input layer from tentacular nerves) of the procerebrum and also by staining afferent nerves immunohistochemically at 15, 58 and 75 days following unilateral amputation of the superior and inferior tentacles. The size of the terminal mass was significantly decreased, and the Phe-Met-Arg-Phe-NH 2 ergic (FMRFamidergic) afferent nerves disappeared by 15 days following the tentacle amputation. However, the size of the terminal mass had recovered substantially by 58 days, as the tentacle regenerated. The FMRFamidergic innervation into the cerebral ganglion was also restored by this time. An extended recovery (75 days), however, did not result in any further increase in the size of the terminal mass. We also recorded the local field potential (LFP) oscillation in the procerebrum. We found that the oscillatory frequency of the LFP had decreased at 15 days following the tentacle amputation but had recovered at 58 and 75 days. These results suggest that the amputation and regrowth of the tentacle are accompanied by the respective degeneration and re-innervation of olfactory nerves, and these changes in the innervation status affect the basal state of LFP oscillation.

show abstract

“…Matsuo et al recently presented data supporting the notion of unilateral memory storage through unilateral procerebrum lesion experiments (Matsuo et al, 2010b). The number of slugs with intact memory performance was reduced by ~50% after the procerebrum was surgically lesioned unilaterally before or after the conditioning.…”

Section: Memory Locus Of Olfactory-aversion Learningmentioning

confidence: 86%

“…This might be enabled by the overall similarity in the structure and cellular components between the superior and inferior tentacles. Such flexibility is, however, restricted to the case when either tentacle is damaged, because selective damages to the unilateral procerebrum result in the reduction of learning performance in that half without compensation by the remaining procerebrum (Matsuo et al, 2010b). In this sense, only the tentacles have functional redundancy for olfactory learning.…”

Section: Discussionmentioning

confidence: 99%

“…Unilateral tentacle amputation experiments (Matsuo et al, 2010b) suggested that the procerebrum ipsilateral to the remaining tentacle is always used for memory storage. These results also support the view that the olfactory projection to the procerebrum from the tentacles is primarily ipsilateral (Chase and Tolloczko, 1989;Matsuo et al, 2010c).…”

Section: Memory Locus Of Olfactory-aversion Learningmentioning

confidence: 99%

See 1 more Smart Citation

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

Matsuo

Kobayashi

Yamagishi

et al. 2011

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Unilateral memory storage in the procerebrum of the terrestrial slug Limax

Cited by 25 publications

References 20 publications

Taste Familiarity Is Inversely Correlated with Arc/Arg3.1 Hemispheric Lateralization

Taste Familiarity Is Inversely Correlated with Arc/Arg3.1 Hemispheric Lateralization

Effects of tentacle amputation and regeneration on the morphology and activity of the olfactory center of the terrestrial slug Limax valentianus

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

Contact Info

Product

Resources

About