IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-35805-9.html
   My bibliography  Save this article

Generalized extinction of fear memory depends on co-allocation of synaptic plasticity in dendrites

Author

Listed:
  • Zhiwei Xu

    (Shenzhen Bay Laboratory
    Peking University Shenzhen Graduate School)

  • Erez Geron

    (New York University School of Medicine)

  • Luis M. Pérez-Cuesta

    (New York University School of Medicine)

  • Yang Bai

    (Peking University Shenzhen Graduate School)

  • Wen-Biao Gan

    (Shenzhen Bay Laboratory
    Peking University Shenzhen Graduate School)

Abstract

Memories can be modified by new experience in a specific or generalized manner. Changes in synaptic connections are crucial for memory storage, but it remains unknown how synaptic changes associated with different memories are distributed within neuronal circuits and how such distributions affect specific or generalized modification by novel experience. Here we show that fear conditioning with two different auditory stimuli (CS) and footshocks (US) induces dendritic spine elimination mainly on different dendritic branches of layer 5 pyramidal neurons in the mouse motor cortex. Subsequent fear extinction causes CS-specific spine formation and extinction of freezing behavior. In contrast, spine elimination induced by fear conditioning with >2 different CS-USs often co-exists on the same dendritic branches. Fear extinction induces CS-nonspecific spine formation and generalized fear extinction. Moreover, activation of somatostatin-expressing interneurons increases the occurrence of spine elimination induced by different CS-USs on the same dendritic branches and facilitates the generalization of fear extinction. These findings suggest that specific or generalized modification of existing memories by new experience depends on whether synaptic changes induced by previous experiences are segregated or co-exist at the level of individual dendritic branches.

Suggested Citation

  • Zhiwei Xu & Erez Geron & Luis M. Pérez-Cuesta & Yang Bai & Wen-Biao Gan, 2023. "Generalized extinction of fear memory depends on co-allocation of synaptic plasticity in dendrites," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35805-9
    DOI: 10.1038/s41467-023-35805-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-35805-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-35805-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Benjamin Scholl & Connon I. Thomas & Melissa A. Ryan & Naomi Kamasawa & David Fitzpatrick, 2021. "Author Correction: Cortical response selectivity derives from strength in numbers of synapses," Nature, Nature, vol. 590(7846), pages 51-51, February.
    2. Hideji Murakoshi & Hong Wang & Ryohei Yasuda, 2011. "Local, persistent activation of Rho GTPases during plasticity of single dendritic spines," Nature, Nature, vol. 472(7341), pages 100-104, April.
    3. Hongbo Jia & Nathalie L. Rochefort & Xiaowei Chen & Arthur Konnerth, 2010. "Dendritic organization of sensory input to cortical neurons in vivo," Nature, Nature, vol. 464(7293), pages 1307-1312, April.
    4. Cora Sau Wan Lai & Thomas F. Franke & Wen-Biao Gan, 2012. "Opposite effects of fear conditioning and extinction on dendritic spine remodelling," Nature, Nature, vol. 483(7387), pages 87-91, March.
    5. Cyril Herry & Stephane Ciocchi & Verena Senn & Lynda Demmou & Christian Müller & Andreas Lüthi, 2008. "Switching on and off fear by distinct neuronal circuits," Nature, Nature, vol. 454(7204), pages 600-606, July.
    6. Xiaowei Chen & Ulrich Leischner & Nathalie L. Rochefort & Israel Nelken & Arthur Konnerth, 2011. "Functional mapping of single spines in cortical neurons in vivo," Nature, Nature, vol. 475(7357), pages 501-505, July.
    7. Andrew J. Peters & Simon X. Chen & Takaki Komiyama, 2014. "Emergence of reproducible spatiotemporal activity during motor learning," Nature, Nature, vol. 510(7504), pages 263-267, June.
    8. Denise J. Cai & Daniel Aharoni & Tristan Shuman & Justin Shobe & Jeremy Biane & Weilin Song & Brandon Wei & Michael Veshkini & Mimi La-Vu & Jerry Lou & Sergio E. Flores & Isaac Kim & Yoshitake Sano & , 2016. "A shared neural ensemble links distinct contextual memories encoded close in time," Nature, Nature, vol. 534(7605), pages 115-118, June.
    9. Guang Yang & Feng Pan & Wen-Biao Gan, 2009. "Stably maintained dendritic spines are associated with lifelong memories," Nature, Nature, vol. 462(7275), pages 920-924, December.
    10. Benjamin Scholl & Connon I. Thomas & Melissa A. Ryan & Naomi Kamasawa & David Fitzpatrick, 2021. "Cortical response selectivity derives from strength in numbers of synapses," Nature, Nature, vol. 590(7844), pages 111-114, February.
    11. Sonja B. Hofer & Thomas D. Mrsic-Flogel & Tobias Bonhoeffer & Mark Hübener, 2009. "Experience leaves a lasting structural trace in cortical circuits," Nature, Nature, vol. 457(7227), pages 313-317, January.
    12. Min Fu & Xinzhu Yu & Ju Lu & Yi Zuo, 2012. "Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo," Nature, Nature, vol. 483(7387), pages 92-95, March.
    13. Christopher D. Harvey & Karel Svoboda, 2007. "Locally dynamic synaptic learning rules in pyramidal neuron dendrites," Nature, Nature, vol. 450(7173), pages 1195-1200, December.
    14. Joseph Cichon & Wen-Biao Gan, 2015. "Branch-specific dendritic Ca2+ spikes cause persistent synaptic plasticity," Nature, Nature, vol. 520(7546), pages 180-185, April.
    15. N. Alex Cayco-Gajic & Claudia Clopath & R. Angus Silver, 2017. "Sparse synaptic connectivity is required for decorrelation and pattern separation in feedforward networks," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    16. N. Toni & P.-A. Buchs & I. Nikonenko & C. R. Bron & D. Muller, 1999. "LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite," Nature, Nature, vol. 402(6760), pages 421-425, November.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Thomas E. Chater & Maximilian F. Eggl & Yukiko Goda & Tatjana Tchumatchenko, 2024. "Competitive processes shape multi-synapse plasticity along dendritic segments," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Matteo Farinella & Daniel T Ruedt & Padraig Gleeson & Frederic Lanore & R Angus Silver, 2014. "Glutamate-Bound NMDARs Arising from In Vivo-like Network Activity Extend Spatio-temporal Integration in a L5 Cortical Pyramidal Cell Model," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-21, April.
    3. Masakazu Agetsuma & Issei Sato & Yasuhiro R. Tanaka & Luis Carrillo-Reid & Atsushi Kasai & Atsushi Noritake & Yoshiyuki Arai & Miki Yoshitomo & Takashi Inagaki & Hiroshi Yukawa & Hitoshi Hashimoto & J, 2023. "Activity-dependent organization of prefrontal hub-networks for associative learning and signal transformation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    4. Michael Fauth & Florentin Wörgötter & Christian Tetzlaff, 2015. "The Formation of Multi-synaptic Connections by the Interaction of Synaptic and Structural Plasticity and Their Functional Consequences," PLOS Computational Biology, Public Library of Science, vol. 11(1), pages 1-29, January.
    5. Najet Serradj & Francesca Marino & Yunuen Moreno-López & Amanda Bernstein & Sydney Agger & Marwa Soliman & Andrew Sloan & Edmund Hollis, 2023. "Task-specific modulation of corticospinal neuron activity during motor learning in mice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Yue Liu & Xiao-Jing Wang, 2024. "Flexible gating between subspaces in a neural network model of internally guided task switching," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    7. Michael Fauth & Florentin Wörgötter & Christian Tetzlaff, 2015. "Formation and Maintenance of Robust Long-Term Information Storage in the Presence of Synaptic Turnover," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-22, December.
    8. Hang Zhou & Guo-Qiang Bi & Guosong Liu, 2024. "Intracellular magnesium optimizes transmission efficiency and plasticity of hippocampal synapses by reconfiguring their connectivity," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Lun Wang & Min Gao & Qinglong Wang & Liyuan Sun & Muhammad Younus & Sixing Ma & Can Liu & Li Shi & Yang Lu & Bo Zhou & Suhua Sun & Guoqing Chen & Jie Li & Quanfeng Zhang & Feipeng Zhu & Changhe Wang &, 2023. "Cocaine induces locomotor sensitization through a dopamine-dependent VTA-mPFC-FrA cortico-cortical pathway in male mice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. Jianian Lin & Zongyue Cheng & Guang Yang & Meng Cui, 2022. "Optical gearbox enabled versatile multiscale high-throughput multiphoton functional imaging," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    11. Qi Wang & Jia-Jie Zhu & Lizhao Wang & Yan-Peng Kan & Yan-Mei Liu & Yan-Jiao Wu & Xue Gu & Xin Yi & Ze-Jie Lin & Qin Wang & Jian-Fei Lu & Qin Jiang & Ying Li & Ming-Gang Liu & Nan-Jie Xu & Michael X. Z, 2022. "Insular cortical circuits as an executive gateway to decipher threat or extinction memory via distinct subcortical pathways," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    12. Francesco Paolo Ulloa Severino & Oluwadamilola O. Lawal & Kristina Sakers & Shiyi Wang & Namsoo Kim & Alexander David Friedman & Sarah Anne Johnson & Chaichontat Sriworarat & Ryan H. Hughes & Scott H., 2023. "Training-induced circuit-specific excitatory synaptogenesis in mice is required for effort control," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    13. Ayush Mandwal & Javier G Orlandi & Christoph Simon & Jörn Davidsen, 2021. "A biochemical mechanism for time-encoding memory formation within individual synapses of Purkinje cells," PLOS ONE, Public Library of Science, vol. 16(5), pages 1-34, May.
    14. Hong Yu & Xinkuan Xiang & Zongming Chen & Xu Wang & Jiaqi Dai & Xinxin Wang & Pengcheng Huang & Zheng-dong Zhao & Wei L. Shen & Haohong Li, 2021. "Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    15. Sravani Kondapavulur & Stefan M. Lemke & David Darevsky & Ling Guo & Preeya Khanna & Karunesh Ganguly, 2022. "Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    16. Sindy Cole & Rick Richardson & Gavan P McNally, 2013. "Ventral Hippocampal Kappa Opioid Receptors Mediate the Renewal of Fear following Extinction in the Rat," PLOS ONE, Public Library of Science, vol. 8(5), pages 1-7, May.
    17. Rodrigo Ordoñez Sierra & Lizeth Katherine Pedraza & Lívia Barcsai & Andrea Pejin & Qun Li & Gábor Kozák & Yuichi Takeuchi & Anett J. Nagy & Magor L. Lőrincz & Orrin Devinsky & György Buzsáki & Antal B, 2023. "Closed-loop brain stimulation augments fear extinction in male rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    18. Caio Vaz Rimoli & Claudio Moretti & Fernando Soldevila & Enora Brémont & Cathie Ventalon & Sylvain Gigan, 2024. "Demixing fluorescence time traces transmitted by multimode fibers," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    19. Devesh Mishra & Nicholas R Harrison & Carolina B Gonzales & Björn Schilström & Åsa Konradsson-Geuken, 2015. "Effects of Age and Acute Ethanol on Glutamatergic Neurotransmission in the Medial Prefrontal Cortex of Freely Moving Rats Using Enzyme-Based Microelectrode Amperometry," PLOS ONE, Public Library of Science, vol. 10(4), pages 1-15, April.
    20. Louis Kang & Taro Toyoizumi, 2024. "Distinguishing examples while building concepts in hippocampal and artificial networks," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35805-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.