IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50388-9.html
   My bibliography  Save this article

Anterior cingulate cortex provides the neural substrates for feedback-driven iteration of decision and value representation

Author

Listed:
  • Wenqi Chen

    (Huazhong University of Science and Technology)

  • Jiejunyi Liang

    (Huazhong University of Science and Technology)

  • Qiyun Wu

    (Huazhong University of Science and Technology)

  • Yunyun Han

    (Huazhong University of Science and Technology)

Abstract

Adjusting decision-making under uncertain and dynamic situations is the hallmark of intelligence. It requires a system capable of converting feedback information to renew the internal value. The anterior cingulate cortex (ACC) involves in error and reward events that prompt switching or maintenance of current decision strategies. However, it is unclear whether and how the changes of stimulus-action mapping during behavioral adaptation are encoded, nor how such computation drives decision adaptation. Here, we tracked ACC activity in male mice performing go/no-go auditory discrimination tasks with manipulated stimulus-reward contingencies. Individual ACC neurons integrate the outcome information to the value representation in the next-run trials. Dynamic recruitment of them determines the learning rate of error-guided value iteration and decision adaptation, forming a non-linear feedback-driven updating system to secure the appropriate decision switch. Optogenetically suppressing ACC significantly slowed down feedback-driven decision switching without interfering with the execution of the established strategy.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50388-9
    DOI: 10.1038/s41467-024-50388-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50388-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-50388-9?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. Albert Tsao & Jørgen Sugar & Li Lu & Cheng Wang & James J. Knierim & May-Britt Moser & Edvard I. Moser, 2018. "Integrating time from experience in the lateral entorhinal cortex," Nature, Nature, vol. 561(7721), pages 57-62, September.
    2. Thomas A. Stalnaker & Nisha K. Cooch & Michael A. McDannald & Tzu-Lan Liu & Heather Wied & Geoffrey Schoenbaum, 2014. "Orbitofrontal neurons infer the value and identity of predicted outcomes," Nature Communications, Nature, vol. 5(1), pages 1-13, September.
    3. Nancy Padilla-Coreano & Kanha Batra & Makenzie Patarino & Zexin Chen & Rachel R. Rock & Ruihan Zhang & Sébastien B. Hausmann & Javier C. Weddington & Reesha Patel & Yu E. Zhang & Hao-Shu Fang & Srisht, 2022. "Cortical ensembles orchestrate social competition through hypothalamic outputs," Nature, Nature, vol. 603(7902), pages 667-671, March.
    4. Junya Hirokawa & Alexander Vaughan & Paul Masset & Torben Ott & Adam Kepecs, 2019. "Frontal cortex neuron types categorically encode single decision variables," Nature, Nature, vol. 576(7787), pages 446-451, December.
    5. Vincent Breton-Provencher & Gabrielle T. Drummond & Jiesi Feng & Yulong Li & Mriganka Sur, 2022. "Spatiotemporal dynamics of noradrenaline during learned behaviour," Nature, Nature, vol. 606(7915), pages 732-738, June.
    6. Seung Wook Oh & Julie A. Harris & Lydia Ng & Brent Winslow & Nicholas Cain & Stefan Mihalas & Quanxin Wang & Chris Lau & Leonard Kuan & Alex M. Henry & Marty T. Mortrud & Benjamin Ouellette & Thuc Ngh, 2014. "A mesoscale connectome of the mouse brain," Nature, Nature, vol. 508(7495), pages 207-214, April.
    7. Nakul Yadav & Chelsea Noble & James E. Niemeyer & Andrea Terceros & Jonathan Victor & Conor Liston & Priyamvada Rajasethupathy, 2022. "Prefrontal feature representations drive memory recall," Nature, Nature, vol. 608(7921), pages 153-160, August.
    8. Abhishek Banerjee & Giuseppe Parente & Jasper Teutsch & Christopher Lewis & Fabian F. Voigt & Fritjof Helmchen, 2020. "Value-guided remapping of sensory cortex by lateral orbitofrontal cortex," Nature, Nature, vol. 585(7824), pages 245-250, September.
    9. 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.
    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. Rebecca J. Rabinovich & Daniel D. Kato & Randy M. Bruno, 2022. "Learning enhances encoding of time and temporal surprise in mouse primary sensory cortex," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Kyuhyun Choi & Eugenio Piasini & Edgar Díaz-Hernández & Luigim Vargas Cifuentes & Nathan T. Henderson & Elizabeth N. Holly & Manivannan Subramaniyan & Charles R. Gerfen & Marc V. Fuccillo, 2023. "Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    3. Luis M. Franco & Michael J. Goard, 2024. "Differential stability of task variable representations in retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Babak Shahbaba & Lingge Li & Forest Agostinelli & Mansi Saraf & Keiland W. Cooper & Derenik Haghverdian & Gabriel A. Elias & Pierre Baldi & Norbert J. Fortin, 2022. "Hippocampal ensembles represent sequential relationships among an extended sequence of nonspatial events," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Wen-Hao Zhang & Si Wu & Krešimir Josić & Brent Doiron, 2023. "Sampling-based Bayesian inference in recurrent circuits of stochastic spiking neurons," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. Alessandra Griffa & Mathieu Mach & Julien Dedelley & Daniel Gutierrez-Barragan & Alessandro Gozzi & Gilles Allali & Joanes Grandjean & Dimitri Ville & Enrico Amico, 2023. "Evidence for increased parallel information transmission in human brain networks compared to macaques and male mice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Anthony Renard & Evan R. Harrell & Brice Bathellier, 2022. "Olfactory modulation of barrel cortex activity during active whisking and passive whisker stimulation," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. Marcus N. Leiwe & Satoshi Fujimoto & Toshikazu Baba & Daichi Moriyasu & Biswanath Saha & Richi Sakaguchi & Shigenori Inagaki & Takeshi Imai, 2024. "Automated neuronal reconstruction with super-multicolour Tetbow labelling and threshold-based clustering of colour hues," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    9. 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.
    10. Xiaxia Xu & Lingzhen Song & Rebecca Kringel & Ileana L. Hanganu-Opatz, 2021. "Developmental decrease of entorhinal-hippocampal communication in immune-challenged DISC1 knockdown mice," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    11. 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.
    12. Marghoti, Gabriel & de Lima Prado, Thiago & Conte, Arturo Cagnato & Ferrari, Fabiano Alan Serafim & Lopes, Sergio Roberto, 2022. "Intermittent chimera-like and bi-stable synchronization states in network of distinct Izhikevich neurons," Chaos, Solitons & Fractals, Elsevier, vol. 162(C).
    13. Yuwen Chen & Haoyu Yang & Yan Luo & Yijun Niu & Muzhou Yu & Shanjun Deng & Xuanhao Wang & Handi Deng & Haichao Chen & Lixia Gao & Xinjian Li & Pingyong Xu & Fudong Xue & Jing Miao & Song-Hai Shi & Yi , 2024. "Photoacoustic Tomography with Temporal Encoding Reconstruction (PATTERN) for cross-modal individual analysis of the whole brain," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    14. Vincent Paget-Blanc & Marlene E. Pfeffer & Marie Pronot & Paul Lapios & Maria-Florencia Angelo & Roman Walle & Fabrice P. Cordelières & Florian Levet & Stéphane Claverol & Sabrina Lacomme & Mélina Pet, 2022. "A synaptomic analysis reveals dopamine hub synapses in the mouse striatum," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    15. Nicholas Cole & Matthew Harvey & Dylan Myers-Joseph & Aditya Gilra & Adil G. Khan, 2024. "Prediction-error signals in anterior cingulate cortex drive task-switching," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    16. Joao Barbosa & Rémi Proville & Chris C. Rodgers & Michael R. DeWeese & Srdjan Ostojic & Yves Boubenec, 2023. "Early selection of task-relevant features through population gating," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    17. Dheeraj S. Roy & Young-Gyun Park & Minyoung E. Kim & Ying Zhang & Sachie K. Ogawa & Nicholas DiNapoli & Xinyi Gu & Jae H. Cho & Heejin Choi & Lee Kamentsky & Jared Martin & Olivia Mosto & Tomomi Aida , 2022. "Brain-wide mapping reveals that engrams for a single memory are distributed across multiple brain regions," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. 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.
    19. Kiyohito Iigaya & Sanghyun Yi & Iman A. Wahle & Sandy Tanwisuth & Logan Cross & John P. O’Doherty, 2023. "Neural mechanisms underlying the hierarchical construction of perceived aesthetic value," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    20. Harry Carey & Michael Pegios & Lewis Martin & Chris Saleeba & Anita J. Turner & Nicholas A. Everett & Ingvild E. Bjerke & Maja A. Puchades & Jan G. Bjaalie & Simon McMullan, 2023. "DeepSlice: rapid fully automatic registration of mouse brain imaging to a volumetric atlas," Nature Communications, Nature, vol. 14(1), pages 1-11, 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:15:y:2024:i:1:d:10.1038_s41467-024-50388-9. 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.