IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28928-y.html
   My bibliography  Save this article

Gq neuromodulation of BLA parvalbumin interneurons induces burst firing and mediates fear-associated network and behavioral state transition in mice

Author

Listed:
  • Xin Fu

    (Tulane University
    Tulane University)

  • Eric Teboul

    (Tufts University School of Medicine and Graduate School of Biomedical Sciences)

  • Grant L. Weiss

    (Tufts University School of Medicine and Graduate School of Biomedical Sciences)

  • Pantelis Antonoudiou

    (Tufts University School of Medicine and Graduate School of Biomedical Sciences)

  • Chandrashekhar D. Borkar

    (Tulane University
    Tulane University)

  • Jonathan P. Fadok

    (Tulane University
    Tulane University)

  • Jamie Maguire

    (Tufts University School of Medicine and Graduate School of Biomedical Sciences)

  • Jeffrey G. Tasker

    (Tulane University
    Tulane University)

Abstract

Patterned coordination of network activity in the basolateral amygdala (BLA) is important for fear expression. Neuromodulatory systems play an essential role in regulating changes between behavioral states, however the mechanisms underlying this neuromodulatory control of transitions between brain and behavioral states remain largely unknown. We show that chemogenetic Gq activation and α1 adrenoreceptor activation in mouse BLA parvalbumin (PV) interneurons induces a previously undescribed, stereotyped phasic bursting in PV neurons and time-locked synchronized bursts of inhibitory postsynaptic currents and phasic firing in BLA principal neurons. This Gq-coupled receptor activation in PV neurons suppresses gamma oscillations in vivo and in an ex vivo slice model, and facilitates fear memory recall, which is consistent with BLA gamma suppression during conditioned fear expression. Thus, here we identify a neuromodulatory mechanism in PV inhibitory interneurons of the BLA which regulates BLA network oscillations and fear memory recall.

Suggested Citation

  • Xin Fu & Eric Teboul & Grant L. Weiss & Pantelis Antonoudiou & Chandrashekhar D. Borkar & Jonathan P. Fadok & Jamie Maguire & Jeffrey G. Tasker, 2022. "Gq neuromodulation of BLA parvalbumin interneurons induces burst firing and mediates fear-associated network and behavioral state transition in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28928-y
    DOI: 10.1038/s41467-022-28928-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28928-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-28928-y?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. 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.
    2. Vasiliki Kanta & Denis Pare & Drew B. Headley, 2019. "Closed-loop control of gamma oscillations in the amygdala demonstrates their role in spatial memory consolidation," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    3. Minagi Ozawa & Patrick Davis & Jianguang Ni & Jamie Maguire & Thomas Papouin & Leon Reijmers, 2020. "Experience-dependent resonance in amygdalo-cortical circuits supports fear memory retrieval following extinction," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    4. Vikaas S. Sohal & Feng Zhang & Ofer Yizhar & Karl Deisseroth, 2009. "Parvalbumin neurons and gamma rhythms enhance cortical circuit performance," Nature, Nature, vol. 459(7247), pages 698-702, June.
    5. Scott F. Owen & Sebnem N. Tuncdemir & Patrick L. Bader & Natasha N. Tirko & Gord Fishell & Richard W. Tsien, 2013. "Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons," Nature, Nature, vol. 500(7463), pages 458-462, August.
    6. Jessica A. Cardin & Marie Carlén & Konstantinos Meletis & Ulf Knoblich & Feng Zhang & Karl Deisseroth & Li-Huei Tsai & Christopher I. Moore, 2009. "Driving fast-spiking cells induces gamma rhythm and controls sensory responses," Nature, Nature, vol. 459(7247), pages 663-667, June.
    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. Sorinel A Oprisan & Xandre Clementsmith & Tamas Tompa & Antonieta Lavin, 2019. "Dopamine receptor antagonists effects on low-dimensional attractors of local field potentials in optogenetic mice," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-39, October.
    2. Huiling Yu & Liping Chen & Huiyang Lei & Guilin Pi & Rui Xiong & Tao Jiang & Dongqin Wu & Fei Sun & Yang Gao & Yuanhao Li & Wenju Peng & Bingyu Huang & Guoda Song & Xin Wang & Jingru Lv & Zetao Jin & , 2022. "Infralimbic medial prefrontal cortex signalling to calbindin 1 positive neurons in posterior basolateral amygdala suppresses anxiety- and depression-like behaviours," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Lou T. Blanpain & Eric R. Cole & Emily Chen & James K. Park & Michael Y. Walelign & Robert E. Gross & Brian T. Cabaniss & Jon T. Willie & Annabelle C. Singer, 2024. "Multisensory flicker modulates widespread brain networks and reduces interictal epileptiform discharges," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    4. Hironobu Osaki & Moeko Kanaya & Yoshifumi Ueta & Mariko Miyata, 2022. "Distinct nociception processing in the dysgranular and barrel regions of the mouse somatosensory cortex," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Yu-Jun Wang & Gui-Ying Zan & Cenglin Xu & Xue-Ping Li & Xuelian Shu & Song-Yu Yao & Xiao-Shan Xu & Xiaoyun Qiu & Yexiang Chen & Kai Jin & Qi-Xin Zhou & Jia-Yu Ye & Yi Wang & Lin Xu & Zhong Chen & Jing, 2023. "The claustrum-prelimbic cortex circuit through dynorphin/κ-opioid receptor signaling underlies depression-like behaviors associated with social stress etiology," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. 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.
    7. Tommaso Ianni & Sedona N. Ewbank & Marjorie R. Levinstein & Matine M. Azadian & Reece C. Budinich & Michael Michaelides & Raag D. Airan, 2024. "Sex dependence of opioid-mediated responses to subanesthetic ketamine in rats," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. 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.
    9. 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.
    10. Hidenori Tabata & Megumi Sasaki & Masakazu Agetsuma & Hitomi Sano & Yuki Hirota & Michio Miyajima & Kanehiro Hayashi & Takao Honda & Masashi Nishikawa & Yutaka Inaguma & Hidenori Ito & Hirohide Takeba, 2022. "Erratic and blood vessel-guided migration of astrocyte progenitors in the cerebral cortex," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    11. Federico Rocchi & Carola Canella & Shahryar Noei & Daniel Gutierrez-Barragan & Ludovico Coletta & Alberto Galbusera & Alexia Stuefer & Stefano Vassanelli & Massimo Pasqualetti & Giuliano Iurilli & Ste, 2022. "Increased fMRI connectivity upon chemogenetic inhibition of the mouse prefrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Emma Leishman & Brian F O’Donnell & James B Millward & Jenifer L Vohs & Olga Rass & Giri P Krishnan & Amanda R Bolbecker & Sandra L Morzorati, 2015. "Phencyclidine Disrupts the Auditory Steady State Response in Rats," PLOS ONE, Public Library of Science, vol. 10(8), pages 1-20, August.
    13. Daigo Takeuchi & Dheeraj Roy & Shruti Muralidhar & Takashi Kawai & Andrea Bari & Chanel Lovett & Heather A. Sullivan & Ian R. Wickersham & Susumu Tonegawa, 2022. "Cingulate-motor circuits update rule representations for sequential choice decisions," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    14. David Wolf & Renée Hartig & Yi Zhuo & Max F. Scheller & Mirko Articus & Marcel Moor & Valery Grinevich & Christiane Linster & Eleonora Russo & Wolfgang Weber-Fahr & Jonathan R. Reinwald & Wolfgang Kel, 2024. "Oxytocin induces the formation of distinctive cortical representations and cognitions biased toward familiar mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    15. Stefano Berto & Alex H. Treacher & Emre Caglayan & Danni Luo & Jillian R. Haney & Michael J. Gandal & Daniel H. Geschwind & Albert A. Montillo & Genevieve Konopka, 2022. "Association between resting-state functional brain connectivity and gene expression is altered in autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    16. Eric Lowet & Krishnakanth Kondabolu & Samuel Zhou & Rebecca A. Mount & Yangyang Wang & Cara R. Ravasio & Xue Han, 2022. "Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    17. Vadivel, R. & Hammachukiattikul, P. & Gunasekaran, Nallappan & Saravanakumar, R. & Dutta, Hemen, 2021. "Strict dissipativity synchronization for delayed static neural networks: An event-triggered scheme," Chaos, Solitons & Fractals, Elsevier, vol. 150(C).
    18. Li, Jiajia & Zhang, Xuan & Du, Mengmeng & Wu, Ying, 2022. "Switching behavior of the gamma power in the neuronal network modulated by the astrocytes," Chaos, Solitons & Fractals, Elsevier, vol. 159(C).
    19. Ankita Sengupta & Sanjna Banerjee & Suhas Ganesh & Shrey Grover & Devarajan Sridharan, 2024. "The right posterior parietal cortex mediates spatial reorienting of attentional choice bias," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    20. Nozomu H. Nakamura & Hidemasa Furue & Kenta Kobayashi & Yoshitaka Oku, 2023. "Hippocampal ensemble dynamics and memory performance are modulated by respiration during encoding," Nature Communications, Nature, vol. 14(1), pages 1-17, 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:13:y:2022:i:1:d:10.1038_s41467-022-28928-y. 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.