Etsuro Ito

Tokushima Bunri University, Tokusima, Tokushima, Japan

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Publications (188)446.93 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: Acetylcholine plays various important roles in the central nervous system of invertebrates as well as vertebrates. In the olfactory center of the terrestrial slug Limax, the local field potential (LFP) oscillates, and the change in its oscillatory frequency is thought to correlate with the detection of odor that potentially changes an ongoing behavior of the animal. Acetylcholine is known to up-regulate the frequency of the LFP oscillation, and is one of the candidates for the neurotransmitters that are involved in such higher cognitive functions. However, there have been no histological data on the cholinergic system in gastropods, nor are there data on the receptors that are responsible for the up-regulation of the oscillatory frequency of LFP due to the lack of analytical tools (such as antibodies or cDNA sequence information of cholinergic system-related genes). Here we cloned the cDNAs of choline acetyltransferase (ChAT), acetylcholinesterase, vesicular acetylcholine transporter, and several nicotinic acetylcholine receptors (nAChRs), and investigated their localization in the brain of Limax. We also generated a polyclonal antibody against ChAT to examine its localization, and investigated pharmacologically the involvement of nAChRs in the LFP oscillation. Our data showed: (1) dense distribution of the neurons expressing mRNAs of ChAT and vesicular acetylcholine transporter in the olfactory center; (2) spatially unique expression patterns of different nAChRs in the olfactory center; (3) involvement of nAChRs in the up-regulation of the oscillation; (4) localization of ChAT protein in nerve fibers and/or terminals; and (5) the presence of cholinergic nerves in the tentacles. J. Comp. Neurol., 2014. © 2014 Wiley Periodicals, Inc.
    The Journal of Comparative Neurology 02/2014; · 3.66 Impact Factor
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    ABSTRACT: The honeybee waggle dance communicates the location of profitable food sources, usually with a certain degree of error in the directional information ranging from 10-15° at the lower margin. We simulated one-day colonial foraging to address the biological significance of information error in the waggle dance. When the error was 30° or larger, the waggle dance was not beneficial. If the error was 15°, the waggle dance was beneficial when the food sources were scarce. When the error was 10° or smaller, the waggle dance was beneficial under all the conditions tested. Our simulation also showed that precise information (0-5° error) yielded great success in finding feeders, but also caused failures at finding new feeders, i.e., a high-risk high-return strategy. The observation that actual bees perform the waggle dance with an error of 10-15° might reflect, at least in part, the maintenance of a successful yet risky foraging trade-off.
    Scientific Reports 01/2014; 4:4175. · 5.08 Impact Factor
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    ABSTRACT: The pond snail Lymnaea stagnalis is capable of being classically conditioned to avoid food and to consolidate this aversion into a long-term memory (LTM). Previous studies have shown that the length of food deprivation is important for both the acquisition of taste aversion and its consolidation into LTM, which is referred to as conditioned taste aversion (CTA). Here we tested the hypothesis that the hemolymph glucose concentration is an important factor in the learning and memory of CTA. One-day food deprivation resulted in the best learning and memory, whereas more prolonged food deprivation had diminishing effects. Five-day food deprivation resulted in snails incapable of learning or remembering. During this food deprivation period, the hemolymph glucose concentration decreased. If snails were fed for 2 days following the 5-day food deprivation, their glucose levels increased significantly and they exhibited both learning and memory, but neither learning nor memory was as good as with the 1-day food-deprived snails. Injection of the snails with insulin to reduce glucose levels resulted in better learning and memory. Insulin is also known to cause a long-term enhancement of synaptic transmission between the feeding-related neurons. On the other hand, injection of glucose into 5-day food-deprived snails did not alter their inability to learn and remember. However, if these snails were fed on sucrose for 3 minutes, they then exhibited learning and memory formation. Our data suggest that hemolymph glucose concentration is an important factor in motivating acquisition of CTA in Lymnaea and that the action of insulin in the brain and the feeding behavior are also important factors.
    Neurobiology of Learning and Memory 10/2013; · 3.33 Impact Factor
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    ABSTRACT: The neural circuitry comprising the central pattern generator (CPG) that drives feeding behavior in the great pond snail (Lymnaea stagnalis (L., 1758)) has been worked out. Because the feeding behavior undergoes associative learning and long-term memory (LTM) formation, it provides an excellent opportunity to study the causal neuronal mechanisms of these two processes. In this review, we explore some of the possible causal neuronal mechanisms of associative learning of conditioned taste aversion (CTA) and its subsequent consolidation processes into LTM in L. stagnalis. In the CTA training procedure, a sucrose solution, which evokes a feeding response, is used as the conditioned stimulus (CS) and a potassium chloride solution, which causes a withdrawal response, is used as the unconditioned stimulus (US). The pairing of the CS–US alters both the feeding response of the snail and the function of a pair of higher order interneurons in the cerebral ganglia. Following the acquisition of CTA, the polysynaptic inhibitory synaptic input from the higher order interneurons onto the feeding CPG neurons is enhanced, resulting in suppression of the feeding response. These changes in synaptic efficacy are thought to constitute a "memory trace" for CTA in L. stagnalis. Résumé : Les circuits neuronaux constituant le générateur central de patrons (CPG) qui régit le comportement d'alimentation de la grande limnée (Lymnaea stagnalis (L., 1758)) ont été décrits. Étant donné que le comportement d'alimentation est assujetti à l'apprentissage associatif et à la formation de la mémoire à long terme (LTM), il présente une excellente occasion d'étudier les mécanismes neuronaux causaux de ces deux processus. Dans la présente synthèse, nous examinons certains de mécanismes neuronaux causaux possibles de l'apprentissage associatif de l'aversion gustative conditionnée (CTA) et les processus de consol-idation subséquente associés dans la LTM de L. stagnalis. Dans la procédure d'apprentissage de la CTA, une solution de sucrose, qui provoque une réaction d'alimentation, est utilisée comme stimulus conditionné (CS), et une solution de chlorure de potassium, qui provoque une réaction de retrait, est utilisée comme stimulus non conditionné (US). Le jumelage de CS–US modifie la réaction d'alimentation de l'escargot et la fonction d'une paire d'interneurones d'ordre supérieur dans le ganglion cérébral. Après l'acquisition de la CTA, le signal synaptique inhibiteur polysynaptique des interneurones d'ordre supérieur vers les neurones associés à l'alimentation du CPG est rehaussé, entraînant la suppression de la réaction d'alimentation. Ces changements de l'efficacité synaptique constitueraient une « trace de la mémoire » pour la CTA chez les L. stagnalis. [Traduit par la Rédaction] Mots-clés : aversion gustative conditionnée, alimentation, mémoire à long terme, Lymnaea stagnalis, retrait.
    Canadian Journal of Zoology 06/2013; 91:405-412. · 1.50 Impact Factor
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    ABSTRACT: The pond snail Lymnaea stagnalis learns taste aversion and consolidates it into long-term memory (LTM). This is referred to as conditioned taste aversion (CTA). The superfusion of molluscan insulin-related peptides (MIPs) over the isolated snail brain causes a long-term enhancement of synaptic input between the cerebral giant cell and the B1 buccal motor neuron. This enhancement is hypothesized to underlie CTA. The synaptic enhancement caused by the superfusion of MIPs can be blocked by the application of human insulin receptor antibody, which recognizes the extracellular domain of human insulin receptor and acts as an antagonist even for MIP receptors. An injection of the human insulin receptor antibody into the abdominal cavity of trained snails blocks the consolidation process leading to LTM, even though the snails acquire taste aversion. Here, we examined whether or not taste-aversion training changes the mRNA expression level of MIP receptor in the snail brain and found that it does not. This result, taken together with previous findings, suggest that the MIPs' effect on synaptic function in the snail brain is attributable to a change in the MIP concentration, and not to a change in the mRNA expression level of MIP receptor, which is thought to reflect the number of MIP receptors.
    Communicative & integrative biology 05/2013; 6(3):e23955.
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    ABSTRACT: The brain of gastropod mollusks contains many giant neurons with polyploid genomic DNAs. Such DNAs are generated through repeated DNA endoreplication during body growth. However, it is not known what triggers DNA endoreplication in neurons. There are two possibilities: (1) DNAs are replicated in response to some unknown molecules in the hemolymph that reflect the nutritive status of the animal; or (2) DNAs are replicated in response to some unknown factors that are retrogradely transported through axons from the innervated target organs. We first tested whether hemolymph with rich nutrition could induce DNA endoreplication. We tested whether the transplanted brain exhibits enhanced DNA endoreplication like an endogenous brain does when transplanted into the homocoel of the body of a slug whose body growth is promoted by an increased food supply. However, no enhancement was observed in the frequency of DNA endoreplication when we compared the transplanted brains in the growth-promoted and growth-suppressed host slugs, suggesting that the humoral environment is irrelevant to triggering the body growth-dependent DNA endoreplication. Next, we tested the requirement of target innervation by surgically dissecting a unilateral posterior pedal nerve of an endogenous brain. Substantially lower number of neurons exhibited DNA endoreplication in the pedal ganglion ipsilateral to the dissected nerve. These results support the view that enhanced DNA endoreplication is mediated by target innervation and is not brought about through the direct effect of humoral factors in the hemolymph during body growth. © 2013 Wiley Periodicals, Inc. Develop Neurobiol, 2013.
    Developmental Neurobiology 04/2013; · 4.42 Impact Factor
  • Neuroscience Letters 03/2013; · 2.03 Impact Factor
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    ABSTRACT: Insulin's action in the brain can directly alter cognitive functioning. We have recently shown that molluscan insulin-related peptides are up-regulated following a conditioned taste aversion (CTA) training procedure. In addition, when mammalian insulin is superfused over the isolated Lymnaea central nervous system, it elicits long-term synaptic enhancement at the monosynaptic connection between the cerebral giant cell (CGC) and the buccal 1 (B1) motor neuron. This synaptic enhancement is thought to be a neural correlate of CTA. Here, we examined whether the observed changes in synaptic plasticity were the result of pre- and/or postsynaptic alterations using the paired pulse procedure. The paired pulse ratio was unaltered following insulin application, suggesting that insulin's effects on synaptic plasticity are mediated postsynaptically in the B1 motor neuron. Thus, it was suggested that postsynaptic changes need to be considered when insulin's actions on synaptic plasticity are examined.
    Journal of Experimental Biology 02/2013; · 3.24 Impact Factor
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    ABSTRACT: The pond snail Lymnaea stagnalis is capable of learning taste aversion and consolidating this learning into long-term memory (LTM) that is called conditioned taste aversion (CTA). Previous studies showed that some molluscan insulin-related peptides (MIPs) were upregulated in snails exhibiting CTA. We thus hypothesized that MIPs play an important role in neurons underlying the CTA-LTM consolidation process. To examine this hypothesis, we first observed the distribution of MIP II, a major peptide of MIPs, and MIP receptor and determined the amounts of their mRNAs in the CNS. MIP II was only observed in the light green cells in the cerebral ganglia, but the MIP receptor was distributed throughout the entire CNS, including the buccal ganglia. Next, when we applied exogenous mammalian insulin, secretions from MIP-containing cells or partially purified MIPs, to the isolated CNS, we observed a long-term change in synaptic efficacy (i.e., enhancement) of the synaptic connection between the cerebral giant cell (a key interneuron for CTA) and the B1 motor neuron (a buccal motor neuron). This synaptic enhancement was blocked by application of an insulin receptor antibody to the isolated CNS. Finally, injection of the insulin receptor antibody into the snail before CTA training, while not blocking the acquisition of taste aversion learning, blocked the memory consolidation process; thus, LTM was not observed. These data suggest that MIPs trigger changes in synaptic connectivity that may be correlated with the consolidation of taste aversion learning into CTA-LTM in the Lymnaea CNS.
    Journal of Neuroscience 01/2013; 33(1):371-383. · 6.91 Impact Factor
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    ABSTRACT: A simple spectrophotometric method for the assay of steroid 5α-reductase (5α-SR) was developed in which 5α-dihydrotestosterone (5α-DHT) and 5α-androstane-3α,17β-diol (5α-diol), metabolites formed in the NADPH-dependent reduction of testosterone with enzyme sources of 5α-SR, were measured by enzymatic cycling using 3α-hydroxysteroid dehydrogenase in the presence of excess thionicotinamide-adenine dinucleotide (thio-NAD) and NADH. It was found that 5α-SR activity was proportional to the accumulated thio-NADH having an absorption maximum at 400 nm. Because of the high cycling rate (> 600 cycle per min) and no interference from testosterone, enzymatic cycling can determine the sum of 5α-DHT and 5α-diol at the picomole level without separation from excess testosterone. The present method was readily applicable to the assay of 5α-SR activity of rat liver and prostate microsomes as well as to the assay of inhibitory activity of finasteride, a synthetic inhibitor of 5α-SR.
    Analytical Sciences 01/2013; 29(4):455-9. · 1.57 Impact Factor
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    ABSTRACT: Fluorescence correlation spectroscopy (FCS) is a technique in which measurement of fluorescence intensity fluctuations is used to clarify dynamic molecular interactions within a very small space in a solution containing a small number of fluorescent molecules. The FCS-based analysis gives the average number and average diffusion time of the fluorescent molecules during their passage through a very small space. One advantage of FCS is that physical separation between free and bound fluorescent probes is not required because the properties of fluorescence fluctuations are accounted for. Therefore, when fluorescent probes are bound with proteins by peroxidase and hydrogen peroxide (H2O2), FCS enables us to detect H2O2 with high sensitivity. In addition, because H2O2 is generated by oxidase-catalyzed reactions, a highly sensitive method for detecting H2O2 is applicable to the measurement of low levels of various oxidases and their substrates, such as glucose. We here describe the protocol of a de novo, highly sensitive method for the measurement of H2O2 and glucose using FCS.
    Methods in enzymology 01/2013; 526:135-43. · 1.90 Impact Factor
  • Etsuro Ito, Satoshi Watabe
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    ABSTRACT: We attempted to develop a super high-sensitive measurement for determination of a small amount of protein by combination of ELISA and enzyme cycling methods. Because protein cannot be amplified, we must amplify the signal intensity corresponding to the amount of protein. For this purpose, we noted that an enzyme cycling method could amplify the signal released from ELISA. In our measurement system, we adopted the thio-NAD cycling method as one of the enzyme cycling methods following ELISA. For example, we employed alkaline phosphatase as an enzyme labeled with an antibody and androsterone phosphate as a substrate for the alkaline phosphatase in ELISA. We then applied a dehydrogenase with a coenzyme, thio NAD, to the thio-NAD cycling method. The signal was measured as the absorbance of thio-NADH, which is generated by the dehydrogenase from the substrate, androsterone, and the coenzyme, thio-NAD. Our measurement system showed that the detection limit of alkaline phosphatase reached 10(-20) mol and that the detection limit of a given protein was 10(-18) mol. Our measurement system will be a powerful tool for diagnosis and assessment of the progress of a disease.
    Rinsho byori. The Japanese journal of clinical pathology 11/2012; 60(11):1088-93.
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    ABSTRACT: The synaptology of the cell body layer of the olfactory center, procerebrum, was investigated in two prominent terrestrial pulmonate gastropod species, Helix pomatia and Limax valentianus. In addition, the analysis of the 5-HT-immunoreactive innervation, including ultrastructural level, was performed at high resolution in H. pomatia. A highly complex system of synaptic and non-synaptic connections was found in the procerebrum of both species connected to local neuropil areas of different size. The procerebral (globuli) cell perikarya were richly innervated by varicosities meanwhile the axon profiles also established contacts with each other. Synaptic configurations including convergence, divergence and presynaptic modulation were also revealed. The frequent occurrence of unspecialized but close axo-somatic and axo-axonic membrane contacts referring to the modulatory forms of transmitter release were also accompanied by membrane configurations indicative of active exocytosis. In H. pomatia, the cell mass layer was shown to receive a rich 5-HT-immunoreactive innervation, forming a dense network around the cell bodies. At ultrastructural level, 5-HT-immunoreactive varicosities contacted both cell bodies and different unlabeled axon profiles. Our results suggest that the local neuropil regions in the cell body layer are site of local circuits, which may play a decisive role in olfactory integrative processes bound to the procerebrum. The pattern and form of the 5-HT-immunoreactive innervation of extrinsic origin suggest an overall modulatory role in the cell body layer. The results may serve a basis for considering the role of local intercellular events, connected to microcircuits, within the procerebrum cell body layer involved in oscillation activities.
    Brain Structure and Function 06/2012; · 7.84 Impact Factor
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    ABSTRACT: The brain of gastropod mollusks contains giant neurons whose nuclei are enlarged with a large amount of genomic DNA. Such DNA is produced by repeated endoreplication. We have previously demonstrated that the frequency of the neuronal DNA endoreplication is correlative to the body growth of the adult land slug and to the increase in the amount of transcripts within the neuron. However, it has long been controversial whether the neuronal DNA endoreplication entails whole genome amplification (polyploidy), or whether only the necessary genomic loci are amplified (polyteny, polysomy, or cis-amplification by unequal recombination). In the present study, we adopted two modern techniques - quantitative genomic PCR and 5'-bromodeoxyuridine labeling - to distinguish between these two possibilities. Our results demonstrated that multiple genomic loci were amplified to the same extent irrespective of the transcriptional activities at these loci. Moreover, the visceral giant cell, the biggest neuron in the slug's brain, was estimated to contain approximately 10 000-times as much genomic DNA as the haploid amount. The 5'-bromodeoxyuridine-labeling experiments also revealed a uniform DNA synthesis within the nucleus. These results strongly support the idea that the giant neurons contain a polyploid genome rather than a locus-specific amplified genome.
    Journal of Neurochemistry 06/2012; 122(4):727-37. · 3.97 Impact Factor
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    ABSTRACT: A honeybee informs her nestmates about the location of a profitable food source that she has visited by means of a waggle dance: a round dance and a figure-of-eight dance for a short- and long-distance food source, respectively. Consequently, the colony achieves an effective collection of food. However, it is still not fully understood how much effect the dance behavior has on the food collection, because most of the relevant experiments have been performed only in limited locations under limited experimental conditions. Here, we examined the efficacy of the waggle dances by physically preventing bees from dancing and then analyzing the changes in daily mass of the hive as an index of daily food collection. To eliminate place- and year-specific effects, the experiments were performed under fully natural conditions in three different cities in Japan from mid September to early October in three different years. Because the experiments were performed in autumn, all six of the tested colonies lost mass on most of the experimental days. When the dance was prevented, the daily reduction in mass change was greater than when the dance was allowed, i.e. the dance inhibited the reduction of the hive mass. This indicates that dance is effective for food collection. Furthermore, clear inhibition was observed on the first two days of the experiments; after that, inhibition was no longer evident. This result suggests that the bee colony adapted to the new environment.
    Journal of Experimental Biology 05/2012; 215(Pt 10):1633-41. · 3.24 Impact Factor
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    ABSTRACT: Classical neurotransmitters, such as glutamate and γ-aminobutyric acid (GABA), often have different actions on invertebrate neurons from those reported for vertebrate neurons. In the terrestrial mollusk Limax, glutamate was found to function as an inhibitory transmitter in the procerebrum (PC), but it has not yet been clarified how GABA acts in the PC. We thus examined what effects GABA exerts on PC neurons in the present study. For this purpose, we first applied GABA to isolated PC preparations and recorded postsynaptic currents and potentials in PC neurons. The GABA application reduced the amplitude of inhibitory postsynaptic currents and depolarization-induced outward currents recorded in nonbursting neurons and increased the number of spontaneous spikes of nonbursting neurons. However, direct GABA-induced currents were not observed in either bursting or nonbursting neurons. These results suggest a potential direct effect of GABA on outward currents resulting in enhanced excitability of PC neurons. Next, we measured the change in [Ca(2+)](i) in cultured PC neurons by application of GABA. The GABA application increased spontaneous Ca(2+) events in cultured neurons. These Ca(2+) events were ascribable to the influx of extracellular Ca(2+). We then confirmed the presence of GABA and GABA receptors in the PC. The GABA-like immunoreactivity was observed in the neuropil layers of the PC, and the mRNAs for both GABA(A) and GABA(B) receptors were expressed in the PC. In particular, GABA(B) receptor mRNA, rather than GABA(A), was found to be more abundantly expressed in the PC. These results suggest that GABA functions as an excitatory modulator for PC neurons via mainly GABA(B) receptors.
    Journal of Neurophysiology 05/2012; 108(4):989-98. · 3.30 Impact Factor
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    ABSTRACT: The gating of ion channel of ionotropic glutamate receptors is controlled by the structural change of the ligand-binding domain of GluR2. We examined the roles of residues in the glutamate-binding and cleft-closing mechanisms by molecular dynamics (MD) simulations. A glutamate entered the cleft deeply within the order of nanoseconds and the cleft locked the glutamate completely at 15 ns in an MD run. TYR450 seemed to regulate the orientation of the glutamate upon binding by cation-π interaction. A semi-open state was identified in the free energy profile evaluated with the structures on the spontaneously glutamate-bound and cleft-closed pathway by the unbiased MD simulations for the first time to our knowledge. In the semi-open state, the two sub-domains were bridged by two hydrogen bonds of GLU705 in the sub-domain 2 with TYR732 in the sub-domain 1 and with the glutamate bound to the sub-domain 1 until the transition to the closed state.
    Biophysical chemistry 03/2012; 162:35-44. · 2.28 Impact Factor
  • S Kobayashi, E Ito
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    ABSTRACT: We examined GABAergic modulation on "slow" oscillation (<1.0 Hz) of the procerebrum in the terrestrial mollusk, Limax valentianus. Short application of GABA-receptor agonists slightly increased the frequency of a periodic oscillation in the procerebrum, whereas persistent application decreased it. GABA-receptor antagonists decreased the oscillatory frequency. The GABA-like immunoreactivities were found in the neuropil and the cell body layers of the procerebrum. Because GABAergic inhibition is known to be essential for the generation of "fast" synchronous neuronal oscillation in the CNSs in othre many animals, our present findings are first evidence suggesting that GABA modulates 'slow' oscillation in the CNS.
    Acta Biologica Hungarica 01/2012; 63 Suppl 2:91-5. · 0.50 Impact Factor
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    ABSTRACT: DNA endoreplication is the DNA synthesis without cell division, resulting in the generation of a nucleus containing a larger amount of genomic DNA compared to a normal diploid genome. There are many such giant neurons in the molluscan brain that are generated as a result of repeated endoreplication. However, it has been controversial whether the endoreplication is the whole genome replication (polyploidy) or the local amplification of the genes that are necessary for the neuron's function (polyteny/polysomy). Here in this study, we investigated these two possibilities by (1) immunohistochemical analysis of the distribution of 5'-bromodeoxyuridine incorporated into the nuclei of the brain neurons, and by (2) quantitative genomic PCR directed to two different genes expressed in specific brain regions. Our data supported the view that the DNA endoreplication is the whole genome replication rather than the local amplification of a specific genomic region.
    Acta Biologica Hungarica 01/2012; 63 Suppl 2:171-8. · 0.50 Impact Factor
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    ABSTRACT: The pond snail, Lymnaea stagnalis, is capable of learning conditioned taste aversion (CTA) and consolidating this CTA into long-term memory (LTM). The DNA microarray experiments showed that some of molluscan insulin-related peptides (MIPs) were up-regulated in snails exhibiting CTA-LTM. On the other hand, the electrophysiological experiments showed that application of secretions from the MIPs-containing cells evoked long-term potentiation (LTP) at the synapses between the cerebral giant cell (a key interneuron for CTA) and the B1 motoneuron (a buccal motoneuron). We thus hypothesized that MIPs and MIP receptors play an important role at the synapses, probably underlying the CTA-LTM consolidation process. To examine this hypothesis, we applied the antibody, which recognizes the binding site of mammalian insulin receptors and is thought to cross-react MIP receptors, to the Lymnaea CNS. Our present data showed that an application of the antibody for insulin receptors to the isolated CNS blocked LTP, and that an injection of the antibody into the Lymnaea abdominal cavity inhibited LTM consolidation, but not CTA formation.
    Acta Biologica Hungarica 01/2012; 63 Suppl 2:194-201. · 0.50 Impact Factor

Publication Stats

2k Citations
446.93 Total Impact Points

Institutions

  • 2006–2014
    • Tokushima Bunri University
      • Kagawa School of Pharmaceutical Sciences
      Tokusima, Tokushima, Japan
  • 2012
    • Mitsubishi Tanabe Pharma Corporation
      Ōsaka, Ōsaka, Japan
    • Hungarian Academy of Sciences
      • Department of Experimental Zoology
      Budapest, Budapest fovaros, Hungary
  • 1994–2009
    • Hokkaido University
      • • Department of Biological Sciences (Biology)
      • • Division of Biological Sciences (Biology)
      • • Graduate School of Science
      Sapporo-shi, Hokkaido, Japan
  • 1993–2008
    • Waseda University
      • • Department of Physics
      • • School of Human Sciences
      Tokyo, Tokyo-to, Japan
    • National Institutes of Health
      • Laboratory of Cellular and Molecular Biology
      Bethesda, MD, United States
  • 1998–2000
    • Shinshu University
      • Department of Neuroplasticity
      Shonai, Nagano, Japan