Molecular and neural mechanisms for a memory of sensory stimulus and behavioral choice

• Project/Area Number: 26430007
• Research Category: Grant-in-Aid for Scientific Research (C)
• Allocation Type: Multi-year Fund
• Section: 一般
• Research Field: Neurophysiology / General neuroscience
• Research Institution: The University of Tokyo
• Principal Investigator: KUNITOMO Hirofumi 東京大学, 大学院理学系研究科(理学部), 准教授 (20302812)
• Co-Investigator(Renkei-kenkyūsha): IINO Yuichi 東京大学, 大学院理学系研究科, 教授 (40192471)
• Research Collaborator: SATO Hirofumi 東京大学, 大学院理学系研究科, 研究員 ; PARK ChanH 東京大学, 大学院理学系研究科, 大学院生
• Project Period (FY): 2014-04-01 – 2018-03-31
• Project Status: Completed (Fiscal Year 2017)
• Budget Amount: ¥5,070,000 (Direct Cost: ¥3,900,000、Indirect Cost: ¥1,170,000); Fiscal Year 2016: ¥1,300,000 (Direct Cost: ¥1,000,000、Indirect Cost: ¥300,000); Fiscal Year 2015: ¥1,950,000 (Direct Cost: ¥1,500,000、Indirect Cost: ¥450,000); Fiscal Year 2014: ¥1,820,000 (Direct Cost: ¥1,400,000、Indirect Cost: ¥420,000)
• Keywords: 記憶と学習 / 線虫 / 走化性 / シナプス可塑性 / 学習 / 記憶 / 神経回路 / 塩素チャネル / 化学感覚

Outline of Final Research Achievements

Learning ability is essential for animals to better adapt and survive in variable environment, and such ability is implemented even in animals with simple neural circuit. Salt chemotaxis of the soil nematode Caenorhabditis elegans is a memory-dependent navigation behavior: animals are attracted to the salt concentration at which they have been fed, whereas they avoid it if they have been starved. We characterized the genes and neural mechanisms required for this learning.
Synaptic transmission from the taste receptor neuron ASER to a pair of interneurons AIB has been implicated as the site of modulation in salt chemotaxis learning. We here revealed that the sign of synaptic transmission reverses according to salt experience, which might generate migration toward opposite directions on the salt gradient. Both excitatory and inhibitory transmissions were at least partially glutamatergic and dependent on EAT-4 (VGLUT) that act in ASER and GLR-1 (AMPA receptor) in AIB.

Research Products

• [Journal Article] A Gustatory Neural Circuit of Caenorhabditis elegans Generates Memory-Dependent Behaviors in Na(+) Chemotaxis. (2017)
  • Author(s): Lifang Wang, Hirofumi Sato, Yohsuke Satoh, Masahiro Tomioka, Hirofumi Kunitomo and Yuichi Iino
  • Journal Title: J Neurosci Volume: 37 Issue: 8 Pages: 2097-2111
  • DOI: 10.1523/jneurosci.1774-16.2017
  • Peer Reviewed / Acknowledgement Compliant
• [Journal Article] 線虫の微小神経回路による学習と記憶 (2016)
  • Author(s): 國友博文、飯野雄一
  • Journal Title: 生体の科学 Volume: 67(1) Pages: 17-21
• [Journal Article] Structural basis for Na+ transport mechanism by a light-driven Na+ pump (2015)
  • Author(s): H. E. Kato, K. Inoue, R. Abe-Yoshizumi, Y. Kato, H. Ono, M. Konno, S. Hososhima, T. Ishizuka, M. R. Hoque, H. Kunitomo, J. Ito, S. Yoshizawa, K. Yamashita, M. Takemoto, T. Nishizawa, R. Taniguchi, K. Kogure, A. D. Maturana, Y. Iino, H. Yawo, R. Ishitani, H. Kandori*, O. Nureki*
  • Journal Title: Nature Volume: 未定 Issue: 7550 Pages: 48-53
  • DOI: 10.1038/nature14322
  • Peer Reviewed / Open Access
• [Journal Article] Role of synaptic phosphatidylinositol 3-kinase in a behavioral learning response in C. elegans (2014)
  • Author(s): Ohno H, Kato S, Naito Y, Kunitomo H, Tomioka M, Iino Y.
  • Journal Title: Science Volume: 345 Issue: 6194 Pages: 313-7
  • DOI: 10.1126/science.1250709
  • Peer Reviewed
• [Journal Article] Regulation of Experience-Dependent Bidirectional Chemotaxis by a Neural Circuit Switch in Caenorhabditis elegans (2014)
  • Author(s): Yohsuke Satoh, Hirofumi Sato, Hirofumi Kunitomo, Xianfeng Fei, Koichi Hashimoto, Yuichi Iino
  • Journal Title: The Journal of Neuroscience Volume: 34 Issue: 47 Pages: 15631-15637
  • DOI: 10.1523/jneurosci.1757-14.2014
  • Peer Reviewed
• [Presentation] Understanding how the interneuron AIY mediates salt concentration memory-dependent behavior in C. elegans. (2018)
  • Author(s): Llian Mabardi, Hirofumi Kunitomo, Hirofumi Sato, Yuichi Iino
  • Organizer: CeNeuro 2018 (C. elegans topic meeting: neuronal development, synaptic function & behavior)
  • Int'l Joint Research
• [Presentation] Roles of the CLC chloride channel clh-1 in food-associated salt chemotaxis learning of Caenorhabditis elegans. (2017)
  • Author(s): ChanHyun Park, Yuki Sakurai, Yuichi Iino, Hirofumi Kunitomo
  • Organizer: 21st International C. elegans Meeting
  • Int'l Joint Research
• [Presentation] Long-lasting memory of salt chemotaxis learning in C. elegans. (2017)
  • Author(s): Shuichi Yanagi, Mai Uemura, Yuichi Iino, Hirofumi Kunitomo
  • Organizer: 37th Blankenese Conference
  • Int'l Joint Research
• [Presentation] A gustatory neural circuit for experience-dependent behavioral plasticity. (2017)
  • Author(s): Hirofumi Sato, Hirofumi Kunitomo, Xianfeng Fei, Koichi Hashimoto, Yuichi Iino
  • Organizer: 21st International C. elegans Meeting
  • Int'l Joint Research
• [Presentation] Roles of primary interneurons that regulate memory-dependent salt concentration chemotaxis in C. elegans. (2017)
  • Author(s): Hirofumi Kunitomo, Hirofumi Sato, Yuichi Iino
  • Organizer: 第40回 日本神経科学大会
• [Presentation] Identification of neurons and analysis of the neural circuit involved in the learned salt-avoidance behavior in C. elegans. (2017)
  • Author(s): M.S. Jang, Y. Toyoshima, H. Kunitomo, Y. Iino1
  • Organizer: 21st International C. elegans Meeting
  • Int'l Joint Research
• [Presentation] Identification of neurons and analysis of the neural circuit involved in the learned salt-avoidance behavior in C. elegans (2017)
  • Author(s): Jang Moon-Sun, Yu Toyoshima, Hirofumi Kunitomo, Yuichi Iino
  • Organizer: 第40回 日本神経科学大会
• [Presentation] Roles of the CLC chloride channel CLH-1 in salt chemotaxis learning of Caenorhabditis elegans (2017)
  • Author(s): Park ChanHyun、櫻井裕樹、飯野雄一、國友博文
  • Organizer: ConBio2017
• [Presentation] 線虫 C. elegansの DAG/PKC経路による学習制御機構の解析 (2017)
  • Author(s): 廣木 進吾、田村 成宏、富岡 征大、國友 博文、飯野 雄一
  • Organizer: ConBio2017
• [Presentation] How taste preference is modulated in the nematode (2017)
  • Author(s): Yuichi Iino, Takashi Nagasima, Hirofumi Sato, Jang Moon-Sun, Suzu Oe, Yu Toyoshima, Masahiro Tomioka, Hirofumi Kunitomo, Stephen Wu, Ryo Yoshida, Yuishi Iwasaki, Takeshi Ishihara
  • Organizer: The 16th International Symposium on Molecular and Neural Mechanisms of Taste and Olfactory Perception (YRUF2017/AISCRIB2017)
  • Int'l Joint Research / Invited
• [Presentation] 線虫C. エレガンスの塩濃度の記憶と走化性の分子・神経機構 (2017)
  • Author(s): 國友博文、佐藤博文、飯野雄一
  • Organizer: 次世代脳プロジェクト 冬のシンポジウム
  • Invited
• [Presentation] A Neural Circuit of Caenorhabditis elegans for Memory-Dependent Na+ Chemotaxis (2016)
  • Author(s): L. WANG, M. TOMIOKA, H. KUNITOMO, Y. IINO
  • Organizer: 20th International C. elegans Meeting
  • Place of Presentation: ロサンゼルス（米国）
  • Year and Date: 2016-06-27
  • Int'l Joint Research
• [Presentation] A neural circuit for memory-dependent Na+ chemotaxis dissected in Caenorhabditis elegans (2016)
  • Author(s): Lifang WANG, Hirofumi Sato, Yohsuke Sato, Masahiro Tomioka, Hirofumi Kunitomo, Yuichi Iino
  • Organizer: 17th International Symposium on Olfaction and Taste (ISOT2016)
  • Place of Presentation: パシフィコ横浜（神奈川県・横浜市）
  • Int'l Joint Research
• [Presentation] identification of neurons analysis of the neuronal circuit involved in the learned salt-avoidance behavior in C. elegans (2016)
  • Author(s): Jang Moon-Sun, Yu Toyoshima, Hirofumi Kunitomo, Manami Kanamori, Takayuki Teramoto, Takeshi Ishihara, Yuichi Iino
  • Organizer: 第54回 日本生物物理学会
  • Place of Presentation: つくば国際会議場（茨城県・つくば市）
• [Presentation] 線虫C. elegansのClC型クロライドチャネルclh-1の塩走性学習における機能の解明 (2016)
  • Author(s): Park ChanHyun、櫻井祐樹、飯野 雄一、國友博文
  • Organizer: 第46回日本神経精神薬理学会年会
  • Place of Presentation: ソウル（韓国）
• [Presentation] The ClC chloride channel CLH-1 is required for salt chemotaxis learning of Caenorhabditis elegans (2016)
  • Author(s): ChanHyunPark, Yuki Sakurai, Hirofumi Kunitomo, Yuichi Iino
  • Organizer: CeNeuro2016
  • Place of Presentation: 名古屋大学（愛知県・名古屋市）
  • Int'l Joint Research
• [Presentation] A neural circuit for experience-dependent salt chemotaxis in C. elegans (2016)
  • Author(s): Hirofumi Sato, Hirofumi Kunitomo, Xianfeng Fei, Koichi Hashimoto, Yuichi Iino
  • Organizer: CeNeuro2016
  • Place of Presentation: 名古屋大学（愛知県・名古屋市）
  • Int'l Joint Research
• [Presentation] Roles of the ClC chloride channel clh-1 in salt chemotaxis learning of Caenorhabditis elegans. (2016)
  • Author(s): ChanHyun Park, Yuki Sakurai, Hirofumi Kunitomo, Yuichi Iino
  • Organizer: 第15回国際シンポジウム「味覚嗅覚の分子神経機構」
  • Place of Presentation: 九州大学（福岡県・福岡市）
  • Int'l Joint Research
• [Presentation] A gustatory neural circuit for experience-dependent salt chemotaxis in C. elegans. (2016)
  • Author(s): Hirofumi Sato, Hirofumi Kunitomo, Xianfeng Fei, Koichi Hashimoto, and Yuichi Iino
  • Organizer: NSF-AMED Workshop: Comparative Principles of Brain Architecture and Functions
  • Place of Presentation: サンディエゴ（米国）
  • Int'l Joint Research
• [Presentation] 線虫C.エレガンスの塩濃度の記憶と走化性の分子・神経機構 (2015)
  • Author(s): 國友博文、飯野雄一
  • Organizer: 包括脳冬のシンポジウム
  • Place of Presentation: 学術総合センター（東京都千代田区）
  • Year and Date: 2015-12-19
• [Presentation] Roles of a ClC chloride channel CLH-1, which is required for salt chemotaxis of Caenorhabditis elegans. (2015)
  • Author(s): 桜井裕樹、朴燦賢、飯野雄一、國友博文
  • Organizer: BMB2015
  • Place of Presentation: 神戸国際会議場（兵庫県神戸市）
  • Year and Date: 2015-12-02
• [Presentation] 線虫の化学走性における定位行動の神経機構 (2015)
  • Author(s): 佐藤陽介、佐藤博文、國友博文、飯野雄一
  • Organizer: BMB2015
  • Place of Presentation: 神戸国際会議場（兵庫県神戸市）
  • Year and Date: 2015-12-01
• [Presentation] A gustatory neural circuit for experience-dependent salt chemotaxis in C. elegans (2015)
  • Author(s): Hirofumi Sato, Hirofumi Kunitomo, Xianfeng Fei, Koichi Hashimoto, Yuichi Iino.
  • Organizer: 20th International C. elegans Meeting
  • Place of Presentation: ロサンゼルス（米国）
  • Year and Date: 2015-06-26
  • Int'l Joint Research
• [Presentation] TOR signaling pathway is involved in regulation of salt chemotaxis learning. (2015)
  • Author(s): Naoko Sakai, Masahiro Tomioka, Hayao Ohno, Hirofumi Kunitomo, Yuichi Iino.
  • Organizer: 20th International C. elegans Meeting
  • Place of Presentation: ロサンゼルス（米国）
  • Year and Date: 2015-06-26
  • Int'l Joint Research
• [Presentation] Dissecting the roles of primary interneurons that regulate memory-dependent salt concentration chemotaxis. (2015)
  • Author(s): Hirofumi Kunitomo, Hirofumi Sato, Yohsuke Satoh, and Yuichi Iino.
  • Organizer: 20th International C. elegans Meeting
  • Place of Presentation: ロサンゼルス（米国）
  • Year and Date: 2015-06-25
  • Int'l Joint Research
• [Presentation] 線虫C. elegans を用いた塩走性学習の長期記憶形成 (2014)
  • Author(s): 植村 舞、飯野 雄一、國友 博文
  • Organizer: 第37回日本分子生物学会年会
  • Place of Presentation: パシフィコ横浜（神奈川県・横浜市）
  • Year and Date: 2014-11-25
• [Presentation] 線虫C. elegans の塩濃度学習におけるモノアミン神経伝達物質の働き (2014)
  • Author(s): 川崎 瑞己、國友 博文、飯野 雄一
  • Organizer: 第37回日本分子生物学会年会
  • Place of Presentation: パシフィコ横浜（神奈川県・横浜市）
  • Year and Date: 2014-11-25
• [Presentation] 線虫の経験塩濃度依存的な行動を制御する神経回路の解明 (2014)
  • Author(s): 佐藤博文、國友博文、Xianfeng Fei、橋本浩一、飯野雄一
  • Organizer: 第37回 日本分子生物学会年会
  • Place of Presentation: パシフィコ横浜（神奈川県・横浜市）
  • Year and Date: 2014-11-25
• [Presentation] Dissecting the roles of primary interneurons that regulate memory-dependent navigation behavior in C. elegans. (2014)
  • Author(s): Hirofumi Kunitomo, Yohsuke Satoh, Hirofumi Sato, Yuichi Iino
  • Organizer: Cold Spring Harbor Asia Conference, Neurobiology: Diverse Species & Conserved Principles
  • Place of Presentation: 蘇州（中国）
  • Year and Date: 2014-09-17
• [Presentation] Neural basis of plasticity and bidirectionality of klinotaxis (2014)
  • Author(s): Yohsuke Satoh, Hirofumi Sato, Hirofumi Kunitomo, Yuichi Iino
  • Organizer: 2014 C. elegans Development, Cell Biology & Gene Expression Meeting in association with The 6th Asia-Pacific C. elegans Meeting
  • Place of Presentation: 奈良県新公会堂（奈良県・奈良市）
  • Year and Date: 2014-07-08
• [Presentation] Identification of molecules downstream of the insulin/PI3K pathway involved in the regulation of salt chemotaxis learning (2014)
  • Author(s): Naoko Sakai, Masahiro Tomioka, Takeshi Adachi, Hirofumi Kunitomo, Yuichi Iino
  • Organizer: 2014 C. elegans topic meeting: Neuronal Development, Synaptic Function and behavior
  • Place of Presentation: マディソン（米国）
  • Year and Date: 2014-07-08