The role of interaction between brain areas on the memory allocation

• Project/Area Number: 17K19638
• Research Category: Grant-in-Aid for Challenging Research (Exploratory)
• Allocation Type: Multi-year Fund
• Research Field: Brain sciences and related fields
• Research Institution: Tokyo University of Science
• Principal Investigator: Sano Yoshitake 東京理科大学, 理工学部応用生物科学科, 講師 (90415175)
• Project Period (FY): 2017-06-30 – 2020-03-31
• Project Status: Completed (Fiscal Year 2019)
• Budget Amount: ¥6,500,000 (Direct Cost: ¥5,000,000、Indirect Cost: ¥1,500,000); Fiscal Year 2018: ¥3,120,000 (Direct Cost: ¥2,400,000、Indirect Cost: ¥720,000); Fiscal Year 2017: ¥3,380,000 (Direct Cost: ¥2,600,000、Indirect Cost: ¥780,000)
• Keywords: 領域間相互作用 / 島皮質 / 扁桃体 / 味覚 / 記憶 / 大脳皮質 / 学習 / セルアッセンブリ / メモリーアロケーション

Outline of Final Research Achievements

To address the cellular mechanism of memory allocation in the insular cortex (IC) and amygdala in the taste memory formation, and its interaction during learning, we manipulated neuronal activity in a subset of IC and/or amygdala neurons using an hM3Dq designer receptor exclusively activated by a designer drug system (DREADD) during conditioned taste aversion (CTA) learning. Then, we have tested whether pre-activated neuronal population were preferentially activated during memory retrieval. When an hM3Dq receptor was activated only in a subset of IC neurons, c-fos expression following memory retrieval was not preferentially observed in hM3Dq+ neurons. Interestingly, the probability of c-fos expression in hM3Dq-positive IC neurons after retrieval was significantly increased when the IC and amygdala were coactivated during conditioning. Our findings suggest that functional interactions between the IC and amygdala neurons regulates CTA memory allocation in the insular cortex.

Academic Significance and Societal Importance of the Research Achievements

日々起きる出来事のいくつかは我々の脳に記憶として蓄えられる。脳は単一の機能を持つ組織ではなく、領域毎に機能が細分化されている。そして出来事を構成する各要素は対応する脳領域で情報が処理、統合され記憶される。一方、記憶を保存する細胞群が、異なる脳領域間でどのような相互作用によりに選択され、記憶ネットワークを形成するのか、その神経基盤は十分に明らかとなっていない。本成果は、記憶形成を担う細胞群を学習時に決定する領域間での相互作用機構を示す重要な発見であるとともに、機能的に細分化された脳が領域間でどのように情報処理を担い協調的に働くかを理解するための糸口を与えると考える。

Research Products

• [Journal Article] Cortico-amygdala interaction determines the insular cortical neurons involved in taste memory retrieval (2020)
  • Author(s): Abe Konami、Kuroda Marin、Narumi Yosuke、Kobayashi Yuki、Itohara Shigeyoshi、Furuichi Teiichi、Sano Yoshitake
  • Journal Title: Molecular Brain Volume: 13 Issue: 1 Pages: 107-107
  • DOI: 10.1186/s13041-020-00646-w
  • Peer Reviewed / Open Access
• [Journal Article] Excitation of prefrontal cortical neurons during conditioning enhances fear memory formation (2020)
  • Author(s): Shibano Natsumi、Yamazaki Mio、Arima Tomoki、Abe Konami、Kuroda Marin、Kobayashi Yuki、Itohara Shigeyoshi、Furuichi Teiichi、Sano Yoshitake
  • Journal Title: Scientific Reports Volume: 10 Issue: 1 Pages: 8613-8613
  • DOI: 10.1038/s41598-020-65597-7
  • Peer Reviewed / Open Access
• [Journal Article] Comparative gene expression analysis of the engulfment and cell motility (ELMO) protein family in the mouse brain (2019)
  • Author(s): Sato Yumi、Sato Akira、Mizuno Shota、Hirota Jun-na、Fujima Shuhei、Ishii Chiaki、Sano Yoshitake、Furuichi Teiichi
  • Journal Title: Gene Expression Patterns Volume: 34 Pages: 119070-119070
  • DOI: 10.1016/j.gep.2019.119070
  • Peer Reviewed
• [Journal Article] Rubber tail illusion is weakened in Ca2+-dependent activator protein for secretion 2 (Caps2)-knockout mice (2019)
  • Author(s): Wada Makoto、Ide Masakazu、Atsumi Takeshi、Sano Yoshitake、Shinoda Yo、Furuichi Teiichi、Kansaku Kenji
  • Journal Title: Scientific Reports Volume: 9 Issue: 1 Pages: 7552-7552
  • DOI: 10.1038/s41598-019-43996-9
  • Peer Reviewed / Open Access
• [Journal Article] Artificial association of memory events by optogenetic stimulation of hippocampal CA3 cell ensembles (2019)
  • Author(s): Oishi Naoya、Nomoto Masanori、Ohkawa Noriaki、Saitoh Yoshito、Sano Yoshitake、Tsujimura Shuhei、Nishizono Hirofumi、Matsuo Mina、Muramatsu Shin-ichi、Inokuchi Kaoru
  • Journal Title: Molecular Brain Volume: 12 Issue: 1 Pages: 111111-111111
  • DOI: 10.1186/s13041-018-0424-1
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] 記憶する細胞を決めるメカニズム (2019)
  • Author(s): 佐野良威、阿部こなみ、柴野奈津美
  • Journal Title: 月刊「細胞」 Volume: -
• [Journal Article] Aspects of excitatory/inhibitory synapses in multiple brain regions are correlated with levels of brain-derived neurotrophic factor/neurotrophin-3 (2019)
  • Author(s): Shinoda Yo、Sadakata Tetsushi、Yagishita Kaori、Kinameri Emi、Katoh-Semba Ritsuko、Sano Yoshitake、Furuichi Teiichi
  • Journal Title: Biochemical and Biophysical Research Communications Volume: 509 Issue: 2 Pages: 429-434
  • DOI: 10.1016/j.bbrc.2018.12.100
  • Peer Reviewed
• [Journal Article] CREB controls cortical circuit plasticity and functional recovery after stroke (2018)
  • Author(s): Caracciolo L.、Marosi M.、Mazzitelli J.、Latifi S.、Sano Y.、Galvan L.、Kawaguchi R.、Holley S.、Levine M. S.、Coppola G.、Portera-Cailliau C.、Silva A. J.、Carmichael S. T.
  • Journal Title: Nature Communications Volume: 9 Issue: 1
  • DOI: 10.1038/s41467-018-04445-9
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Calcium-dependent activator protein for secretion 2 (CADPS2) deficiency causes abnormal synapse development in hippocampal mossy fiber terminals (2018)
  • Author(s): Shinoda Yo、Sadakata Tetsushi、Akagi Takumi、Sakamaki Yuriko、Hashikawa Tsutomu、Sano Yoshitake、Furuichi Teiichi
  • Journal Title: Neuroscience Letters Volume: 677 Pages: 65-71
  • DOI: 10.1016/j.neulet.2018.04.036
  • Peer Reviewed
• [Journal Article] CAPS2 deficiency affects environmental enrichment-induced adult neurogenesis and differentiation/survival of newborn neurons in the hippocampal dentate gyrus (2017)
  • Author(s): Yagishita Kaori、Suzuki Ritsuko、Mizuno Shota、Katoh-Semba Ritsuko、Sadakata Tetsushi、Sano Yoshitake、Furuichi Teiichi、Shinoda Yo
  • Journal Title: Neuroscience Letters Volume: 661 Pages: 121-125
  • DOI: 10.1016/j.neulet.2017.09.047
  • Peer Reviewed
• [Presentation] The role of coordinated activation between insular cortex and basolateral amygdala during taste-aversion association learning to recruit a memory trace. (2019)
  • Author(s): Konami Abe, Marin Kuroda, Yosuke Narumi, Yuki Kobayashi, Shigeyoshi Itohara, Teiichi Furuichi and Yoshitake Sano
  • Organizer: Society for Neuroscience, Neuroscience 2019
  • Int'l Joint Research
• [Presentation] Excitation of medial prefrontal cortex during conditioning enhances fear memory formation. (2019)
  • Author(s): Natsumi Shibano, Mio Yamazaki, Marine Kuroda, Konami Abe, Tomoki Arima, Yuki Kobayashi, Shigeyoshi Itohara, Teiichi Furuichi and Yoshitake Sano.
  • Organizer: Society for Neuroscience, Neuroscience 2019
  • Int'l Joint Research
• [Presentation] A possible involvement of Ca2+-dependent activator protein for secretion 2 (CAPS2) in regulating release of the hypothalamic neuropeptide oxytocin that has a pivotal role in social behavior. (2019)
  • Author(s): Shuhei Fujima, Rina Maniwa, Ryosuke Yamaga, Yoshitake Sano and Teiichi Furuichi.
  • Organizer: Society for Neuroscience, Neuroscience 2019
  • Int'l Joint Research
• [Presentation] Comprehensive profiling and localization of gene expression in the cerebral cortex and striatum of BTBR mice, a mouse model of autism spectrum disorder by comparing with those of C57BL6/J, a highly social mouse strain. (2019)
  • Author(s): Shota Mizuno, Jun-na Hirota, Hirohide Iwasaki, Shigeo Okabe, Yoshitake Sano and Teiichi Furuichi.
  • Organizer: Society for Neuroscience, Neuroscience 2019
  • Int'l Joint Research
• [Presentation] アミロイドβの蓄積による軽度認知機能低下と炎症性免疫反応の亢進 (2019)
  • Author(s): 加藤 優奈, 水野 翔太, 石井 千晶, 山中 琴未, 栄田 浩伸, 村上 祐香, 斉藤 貴志, 西道 隆臣, 古市 貞 一, 佐野 良威
  • Organizer: 第42回 日本分子生物学学会
• [Presentation] 分泌関連タンパク質CAPS2の欠損は自然発症慢性膵炎を引き起こす (2019)
  • Author(s): 佐藤 陽太郎, 露崎 美穂, 志村 拓哉, 小林 りか, 定方 哲史, 佐野 良威, 古市 貞一
  • Organizer: 第92回日本生化学学会
• [Presentation] 自閉症モデルマウスBTBR系統で特異的に発現変動する遺伝子の脳内局在および機能解析 (2019)
  • Author(s): 弘田 淳奈, 水野 翔太, 岩崎 広英, 岡部 繁男, 佐野 良威, 古市 貞一
  • Organizer: 第92回日本生化学学会
• [Presentation] 味覚記憶の形成における階層的領域間相互作用 (2019)
  • Author(s): 阿部 こなみ, 黒田 真鈴, 鳴海 陽介, 小林 祐樹, 糸原 重美, 古市 貞一, ○佐野 良威
  • Organizer: 第92回日本生化学学会
• [Presentation] Comprehensive gene expression profiling between BTBR mice, a mouse model of autism spectrum disorder, and C57BL6/J mice showing high levels of sociality. (2019)
  • Author(s): Shota Mizuno, Junna Hirota, Hirohide Iwasaki, Shigeo Okabe, Yoshitake Sano and Teiichi Furuichi
  • Organizer: NEURO2019
• [Presentation] The role of coordinated activation between insular cortex and basolateral amygdala during taste-aversion association learning to recruit a memory trace (2019)
  • Author(s): Konami Abe, Marin Kuroda, Yosuke Narumi, Yiki Kobayashi, Shigeyoshi Itoahra and Taiichi Furuichi and Yoshitake Sano
  • Organizer: NEURO2019
• [Presentation] Mice lacking Ca2+-dependent activator protein for secretion 2 (CAPS2) show a decrease in oxytocin release and impaired social behavior (2019)
  • Author(s): Shuhei Fujima, Ryosuke Yamaga, Haruka Minami, Rina Maniwa, Yo Shinoda, Manabu Abe, Kenji Sakimura, Yoshitake Sano and Teiichi Furuichi
  • Organizer: NEURO2019
• [Presentation] Decreased social interaction and motivated approach behavior in the X11L-deficient mice (2019)
  • Author(s): Kotomi Yamanaka, Shota Mizuno, Teiichi Furuichi and Yoshitake Sano
  • Organizer: NEURO2019
• [Presentation] Significant role of CAPS1, a regulator of synaptic exocytosis, in trisynaptic circuit and hippocampal learning (2019)
  • Author(s): Tomoki Arima, Chiaki Ishii, Yuki Ishii, Natsumi Shibano, Mio Yamazaki, Yuna Kato, Ami Yamato, Yo Shinoda, Tetsushi Sadakata, Yoshitake Sano and Teiichi Furuichi
  • Organizer: NEURO2019
• [Presentation] Lower c-Fos expressions in the posterior parietal cortex during rubber tail task in Caps2 KO mice (2019)
  • Author(s): Wada M, Ide M, Atsumi T, Takano K, Sano Y, Shinoda Y, Fruichi T, Kansaku K.
  • Organizer: 9th FAOPS
• [Presentation] CAPS1 is critical for hippocampal synaptic transmission and learning. (2018)
  • Author(s): Yoshitake Sano
  • Organizer: 13th International Conference of Neurons and Brain Diseases
  • Int'l Joint Research / Invited
• [Presentation] Synchronous activation of distinct memory ensembles in CA3 integrate two memories. (2018)
  • Author(s): Naoya Oishi, Kohei Koga, Masanori Nomoto, Noriaki Ohkawa, Shuhei Tsujimura, Yoshitake Sano, Yoshito Saitoh, Hirofumi Nishizono, Mina Matsuo, Shin-Ichi Muramatsu, Kaoru Inokuchi
  • Organizer: 生理研研究会
• [Presentation] 海馬における分泌関連因子 CAPS1 の機能解析と記憶・学習への寄与 (2018)
  • Author(s): Chiaki Ishii, Yuki Ishii, Natsumi Shibano, Yuna Kato, Mio Yamazaki, Ami Yamato, Yo Shinoda, Tetsushi Sadakata, Yoshitake Sano and Teiichi Furuichi
  • Organizer: 生理研研究会
• [Presentation] 味覚嫌悪学習における脳領域間相互作用 (2018)
  • Author(s): Konami Abe, Yosuke Narumi, Shuhei Fujima, Yuki Kobayashi, Shigeyoshi Itohara, Teiichi Furuichi, Yoshitake Sano
  • Organizer: 生理研研究会
• [Presentation] The molecular mechanism regulating axonal localization of the secretion-related protein CAPS2. (2018)
  • Author(s): Kazuki Shimizu, Kazuo Kawamoto, Tetsushi Sadakata, Yoshitake Sano, Teiichi Furuichi
  • Organizer: 第61回日本神経化学会大会・第40回日本生物学的精神医学会
• [Presentation] Oxytocin secretion and social behavior in mice lacking Ca2+-dependent activator protein for secretion 2 (CAPS2). Ca2+-dependent activator protein for secretion 2 (2018)
  • Author(s): Shuhei Fujima, Ryousuke Yamaga, Haruka Minami, Rina Maniwa, Yo Shinoda, Manabu Abe, Kenji Sakimura, Yoshitake Sano & Teiichi Furuichi
  • Organizer: Neuroscience 2018
• [Presentation] Establishment of in vivo field excitatory post synaptic potential (fEPSP) recording system at hippocampal CA3-CA3 synapses (2018)
  • Author(s): Naoya Oishi, Kohei Koga, Masanori Nomoto, Noriaki Ohkawa, Shuhei Tsujimura, Yoshitake Sano, Yoshito Saitoh, Hirofumi Nishizono, Mina Matsuo, Shin-Ichi Muramatsu, Kaoru Inokuchi
  • Organizer: Neuroscience 2018
• [Presentation] Interaction between insular cortex and amygdala during a taste aversion association. (2018)
  • Author(s): Konami Abe, Yosuke Narumi, Shuhei Fujima, Yuki Kobayashi, Shigeyoshi Itohara, Teiichi Furuichi, Yoshitake Sano
  • Organizer: Neuroscience 2018
• [Presentation] CAPS1 regulates efficient and/or synchronous exocytosis of releasable synaptic vesicles, which effects on hippocampal synaptic plasticity, learning and memory. (2018)
  • Author(s): Chiaki Ishii, Yuki Ishii, Natsumi Shibano, Yuna Kato, Mio Yamazaki, Ami Yamato, Yo Shinoda, Tetsushi Sadakata, Yoshitake Sano and Teiichi Furuichi
  • Organizer: Neuroscience 2018
• [Presentation] Comparative gene expression profiling between BTBR mice, a mouse model of autism spectrum disorder, and C57BL6/J mice showing high levels of sociality. (2018)
  • Author(s): Shota Mizuno, Chiaki Ishii, Hirohide Iwasaki, Shigeo Okabe, Yoshitake Sano and Teiichi Furuichi
  • Organizer: Neuroscience 2018
• [Presentation] CAPS2 deficiency does not affect social isolation-induced behavioral abnormalities. (2018)
  • Author(s): Mizuki Oka, Tetsushi Sadakata, Yoshitake Sano, Teiichi Furuichi, Yasuyuki Fujiwara, Yo Shinoda
  • Organizer: Neuroscience 2018
• [Presentation] 記憶保存細胞の選択における転写調節因子 CREB の役割 (2018)
  • Author(s): 佐野 良威
  • Organizer: 日本薬学会第138年会
• [Presentation] Oxytocin secretion and social behavior in mice lacking Ca2+-dependent activator protein for secretion 2 (CAPS2) (2018)
  • Author(s): S. FUJIMA, R. MANIWA, Y. SANO, T. FURUICHI
  • Organizer: Neuroscience 2018, Annual Meeting of Society for Neuroscience
  • Int'l Joint Research
• [Presentation] Social isolation-mediated hyperactivity and reduction of anxiety are not affected by Caps2 deficiency (2018)
  • Author(s): Y. SHINODA , M. OKA , N. TANAKA , Y. FUJIWARA , Y. SANO , T. SADAKATA , T. FURUICHI
  • Organizer: Neuroscience 2018, Annual Meeting of Society for Neuroscience
  • Int'l Joint Research
• [Presentation] CAPS1 finely regulates the exocytosis of synaptic vesicles in calcium- and/or synapse type-dependent manners, affecting on learning and memory (2018)
  • Author(s): C. ISHII , Y. SHINODA , T. SADAKATA , Y. SANO , Y. ISHII , N. SHIBANO , Y. KATO , M. YAMAZAKI , A. YAMATO , T. FURUICHI
  • Organizer: Neuroscience 2018, Annual Meeting of Society for Neuroscience
  • Int'l Joint Research
• [Presentation] Lower c-Fos expressions in the posterior parietal cortex during rubber tail task in Caps2 KO mice (2018)
  • Author(s): Wada M, Ide M, Atsumi T, Takano K, Sano Y, Shinoda Y, Fruichi T, Kansaku K.
  • Organizer: 9th FAOPS（第9回アジア・オセアニア生理学会連合大会）＆第96回日本生理学会合同大会
  • Int'l Joint Research
• [Presentation] 記憶保存細胞の選択における転写調節因子CREBの役割 (2018)
  • Author(s): 佐野良威
  • Organizer: 日本薬学会
  • Invited
• [Presentation] Selection of Memory Cells (2017)
  • Author(s): Yoshitake Sano
  • Organizer: International Symposium of the Center for Animal Disease Models 2017
  • Int'l Joint Research / Invited
• [Presentation] 記憶を保存する細胞群を決める機構の解明 (2017)
  • Author(s): 佐野良威
  • Organizer: 第1回 東京理科大学脳学際研究部門公開シンポジウム
  • Invited
• [Presentation] CAPS1 stabilizes synaptic vesicles on active zones and ensures basal synaptic transmission at hippocampal CA3-CA1 synapses (2017)
  • Author(s): Chiaki Ishii, Yo Shinoda, Yugo Fukazawa, Tetsushi Sadakata, Yuki Ishii, Yoshitake Sano, Takuji Iwasato, Shigeyoshi Itohara, and Teiichi Furuichi
  • Organizer: Neuroscience 2017, Society for Neuroscience
• [Presentation] ＣＡＰＳ１はシナプス小胞を活性帯上で安定化させることで海馬ＣＡ３－ＣＡ１シナプスにおいて開口放出を調節する (2017)
  • Author(s): 石井 千晶、篠田 陽、深澤 有吾、定方 哲史、石井 佑季、佐野 良威、岩里 琢治、糸原 重美、古市 貞一
  • Organizer: 第40回日本神経科学大会
• [Presentation] エピソード記憶の形成における分泌関連タンパク質ＣＡＰＳ１の役割 (2017)
  • Author(s): 柴野 奈津美、石井 佑季、佐野 良威、古市 貞一
  • Organizer: 第40回日本神経科学大会
• [Book] Recruiting cell assembly into a given memory trace、記憶する細胞を決めるメカニズム (2019)
  • Author(s): 佐野 良威、阿部 こなみ、柴野 奈津美
  • Total Pages: 5
  • Publisher: 月刊「細胞」北隆館
• [Book] Recruiting cell assembly into a trace of taste-emotion memory. 感覚と情動を記憶する細胞を決める機構 (2019)
  • Author(s): 佐野 良威、阿部 こなみ、柴野 奈津美
  • Total Pages: 5
  • Publisher: アグリバイオ 北隆館