IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26852-1.html
   My bibliography  Save this article

Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice

Author

Listed:
  • Hong Yu

    (Huazhong University of Science and Technology
    Huazhong University of Science and Technology
    Hubei University of Medicine)

  • Xinkuan Xiang

    (Huazhong University of Science and Technology
    Huazhong University of Science and Technology)

  • Zongming Chen

    (Shanghaitech University)

  • Xu Wang

    (Huazhong University of Science and Technology
    Huazhong University of Science and Technology)

  • Jiaqi Dai

    (Huazhong University of Science and Technology
    Huazhong University of Science and Technology)

  • Xinxin Wang

    (Huazhong University of Science and Technology
    Huazhong University of Science and Technology)

  • Pengcheng Huang

    (Huazhong University of Science and Technology
    Huazhong University of Science and Technology)

  • Zheng-dong Zhao

    (Boston Children’s Hospital)

  • Wei L. Shen

    (Shanghaitech University)

  • Haohong Li

    (Huazhong University of Science and Technology
    Huazhong University of Science and Technology
    Zhejiang University School of Medicine
    Zhejiang University School of Brain Science and Brain Medicine)

Abstract

Sequential encoding of motor programs is essential for behavior generation. However, whether it is critical for instinctive behavior is still largely unknown. Mouse hunting behavior typically contains a sequential motor program, including the prey search, chase, attack, and consumption. Here, we reveal that the neuronal activity in the lateral periaqueductal gray (LPAG) follows a sequential pattern and is time-locked to different hunting actions. Optrode recordings and photoinhibition demonstrate that LPAGVgat neurons are required for the prey detection, chase and attack, while LPAGVglut2 neurons are selectively required for the attack. Ablation of inputs that could trigger hunting, including the central amygdala, the lateral hypothalamus, and the zona incerta, interrupts the activity sequence pattern and substantially impairs hunting actions. Therefore, our findings reveal that periaqueductal gray neuronal ensembles encode the sequential hunting motor program, which might provide a framework for decoding complex instinctive behaviors.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26852-1
    DOI: 10.1038/s41467-021-26852-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26852-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-26852-1?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. 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.
    2. Franz Weber & Shinjae Chung & Kevin T. Beier & Min Xu & Liqun Luo & Yang Dan, 2015. "Control of REM sleep by ventral medulla GABAergic neurons," Nature, Nature, vol. 526(7573), pages 435-438, October.
    3. Ben Engelhard & Joel Finkelstein & Julia Cox & Weston Fleming & Hee Jae Jang & Sharon Ornelas & Sue Ann Koay & Stephan Y. Thiberge & Nathaniel D. Daw & David W. Tank & Ilana B. Witten, 2019. "Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons," Nature, Nature, vol. 570(7762), pages 509-513, June.
    4. Philip Tovote & Maria Soledad Esposito & Paolo Botta & Fabrice Chaudun & Jonathan P. Fadok & Milica Markovic & Steffen B. E. Wolff & Charu Ramakrishnan & Lief Fenno & Karl Deisseroth & Cyril Herry & S, 2016. "Midbrain circuits for defensive behaviour," Nature, Nature, vol. 534(7606), pages 206-212, June.
    5. Brad E. Pfeiffer & David J. Foster, 2013. "Hippocampal place-cell sequences depict future paths to remembered goals," Nature, Nature, vol. 497(7447), pages 74-79, May.
    6. Jeremiah Y. Cohen & Sebastian Haesler & Linh Vong & Bradford B. Lowell & Naoshige Uchida, 2012. "Neuron-type-specific signals for reward and punishment in the ventral tegmental area," Nature, Nature, vol. 482(7383), pages 85-88, February.
    7. D. Kvitsiani & S. Ranade & B. Hangya & H. Taniguchi & J. Z. Huang & A. Kepecs, 2013. "Distinct behavioural and network correlates of two interneuron types in prefrontal cortex," Nature, Nature, vol. 498(7454), pages 363-366, June.
    8. Meizhu Huang & Dapeng Li & Xinyu Cheng & Qing Pei & Zhiyong Xie & Huating Gu & Xuerong Zhang & Zijun Chen & Aixue Liu & Yi Wang & Fangmiao Sun & Yulong Li & Jiayi Zhang & Miao He & Yuan Xie & Fan Zhan, 2021. "The tectonigral pathway regulates appetitive locomotion in predatory hunting in mice," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    9. Christopher D. Harvey & Philip Coen & David W. Tank, 2012. "Choice-specific sequences in parietal cortex during a virtual-navigation decision task," Nature, Nature, vol. 484(7392), pages 62-68, April.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Fernando M. C. V. Reis & Sandra Maesta-Pereira & Matthias Ollivier & Peter J. Schuette & Ekayana Sethi & Blake A. Miranda & Emily Iniguez & Meghmik Chakerian & Eric Vaughn & Megha Sehgal & Darren C. T, 2024. "Control of feeding by a bottom-up midbrain-subthalamic pathway," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

    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. Panna Hegedüs & Bálint Király & Dániel Schlingloff & Victoria Lyakhova & Anna Velencei & Írisz Szabó & Márton I. Mayer & Zsofia Zelenak & Gábor Nyiri & Balázs Hangya, 2024. "Parvalbumin-expressing basal forebrain neurons mediate learning from negative experience," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. John Palmer & Adam Keane & Pulin Gong, 2017. "Learning and executing goal-directed choices by internally generated sequences in spiking neural circuits," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-23, July.
    3. Torben Ott & Anna Marlina Stein & Andreas Nieder, 2023. "Dopamine receptor activation regulates reward expectancy signals during cognitive control in primate prefrontal neurons," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Allen P. F. Chen & Jeffrey M. Malgady & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Joshua L. Plotkin & Shaoyu Ge & Qiaojie Xiong, 2022. "Nigrostriatal dopamine pathway regulates auditory discrimination behavior," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Suma Chinta & Scott R. Pluta, 2023. "Neural mechanisms for the localization of unexpected external motion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. Clément Solié & Alessandro Contestabile & Pedro Espinosa & Stefano Musardo & Sebastiano Bariselli & Chieko Huber & Alan Carleton & Camilla Bellone, 2022. "Superior Colliculus to VTA pathway controls orienting response and influences social interaction in mice," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. J Matthew Mahoney & Ali S Titiz & Amanda E Hernan & Rod C Scott, 2016. "Short-Range Temporal Interactions in Sleep; Hippocampal Spike Avalanches Support a Large Milieu of Sequential Activity Including Replay," PLOS ONE, Public Library of Science, vol. 11(2), pages 1-25, February.
    8. Young Hee Lee & Yu-Been Kim & Kyu Sik Kim & Mirae Jang & Ha Young Song & Sang-Ho Jung & Dong-Soo Ha & Joon Seok Park & Jaegeon Lee & Kyung Min Kim & Deok-Hyeon Cheon & Inhyeok Baek & Min-Gi Shin & Eun, 2023. "Lateral hypothalamic leptin receptor neurons drive hunger-gated food-seeking and consummatory behaviours in male mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Coralie Hérent & Séverine Diem & Giovanni Usseglio & Gilles Fortin & Julien Bouvier, 2023. "Upregulation of breathing rate during running exercise by central locomotor circuits in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Marta Huelin Gorriz & Masahiro Takigawa & Daniel Bendor, 2023. "The role of experience in prioritizing hippocampal replay," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    11. Wenqi Chen & Jiejunyi Liang & Qiyun Wu & Yunyun Han, 2024. "Anterior cingulate cortex provides the neural substrates for feedback-driven iteration of decision and value representation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    12. Terence C. Burnham & Jay Phelan, 2020. "Ordinaries," Journal of Bioeconomics, Springer, vol. 22(2), pages 63-76, July.
    13. Nicolas Cazin & Martin Llofriu Alonso & Pablo Scleidorovich Chiodi & Tatiana Pelc & Bruce Harland & Alfredo Weitzenfeld & Jean-Marc Fellous & Peter Ford Dominey, 2019. "Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-32, July.
    14. Elaida D. Dimwamwa & Aurélie Pala & Vivek Chundru & Nathaniel C. Wright & Garrett B. Stanley, 2024. "Dynamic corticothalamic modulation of the somatosensory thalamocortical circuit during wakefulness," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Jun Wang & Qian Yang & Xue Liu & Jie Li & Ya-Lan Wen & Yuzheng Hu & Tian-Le Xu & Shumin Duan & Han Xu, 2024. "The basal forebrain to lateral habenula circuitry mediates social behavioral maladaptation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    16. Athina Tzovara & Christoph W Korn & Dominik R Bach, 2018. "Human Pavlovian fear conditioning conforms to probabilistic learning," PLOS Computational Biology, Public Library of Science, vol. 14(8), pages 1-21, August.
    17. Ami Ritter & Shlomi Habusha & Lior Givon & Shahaf Edut & Oded Klavir, 2024. "Prefrontal control of superior colliculus modulates innate escape behavior following adversity," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. 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.
    19. Ravi Pancholi & Lauren Ryan & Simon Peron, 2023. "Learning in a sensory cortical microstimulation task is associated with elevated representational stability," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    20. Masashi Hasegawa & Ziyan Huang & Ricardo Paricio-Montesinos & Jan Gründemann, 2024. "Network state changes in sensory thalamus represent learned outcomes," Nature Communications, Nature, vol. 15(1), pages 1-14, 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:12:y:2021:i:1:d:10.1038_s41467-021-26852-1. 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.