IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50501-y.html
   My bibliography  Save this article

Flexible gating between subspaces in a neural network model of internally guided task switching

Author

Listed:
  • Yue Liu

    (New York University)

  • Xiao-Jing Wang

    (New York University)

Abstract

Behavioral flexibility relies on the brain’s ability to switch rapidly between multiple tasks, even when the task rule is not explicitly cued but must be inferred through trial and error. The underlying neural circuit mechanism remains poorly understood. We investigated recurrent neural networks (RNNs) trained to perform an analog of the classic Wisconsin Card Sorting Test. The networks consist of two modules responsible for rule representation and sensorimotor mapping, respectively, where each module is comprised of a circuit with excitatory neurons and three major types of inhibitory neurons. We found that rule representation by self-sustained persistent activity across trials, error monitoring and gated sensorimotor mapping emerged from training. Systematic dissection of trained RNNs revealed a detailed circuit mechanism that is consistent across networks trained with different hyperparameters. The networks’ dynamical trajectories for different rules resided in separate subspaces of population activity; the subspaces collapsed and performance was reduced to chance level when dendrite-targeting somatostatin-expressing interneurons were silenced, illustrating how a phenomenological description of representational subspaces is explained by a specific circuit mechanism.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50501-y
    DOI: 10.1038/s41467-024-50501-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50501-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-50501-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. Arghya Mukherjee & Norman H. Lam & Ralf D. Wimmer & Michael M. Halassa, 2021. "Thalamic circuits for independent control of prefrontal signal and noise," Nature, Nature, vol. 600(7887), pages 100-104, December.
    2. Seung-Hee Lee & Alex C. Kwan & Yang Dan, 2014. "Interneuron subtypes and orientation tuning," Nature, Nature, vol. 508(7494), pages 1-2, April.
    3. Valerio Mante & David Sussillo & Krishna V. Shenoy & William T. Newsome, 2013. "Context-dependent computation by recurrent dynamics in prefrontal cortex," Nature, Nature, vol. 503(7474), pages 78-84, November.
    4. 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.
    5. James P. Roach & Anne K. Churchland & Tatiana A. Engel, 2023. "Choice selective inhibition drives stability and competition in decision circuits," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Takuya Ito & Guangyu Robert Yang & Patryk Laurent & Douglas H. Schultz & Michael W. Cole, 2022. "Constructing neural network models from brain data reveals representational transformations linked to adaptive behavior," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Jonathan D. Wallis & Kathleen C. Anderson & Earl K. Miller, 2001. "Single neurons in prefrontal cortex encode abstract rules," Nature, Nature, vol. 411(6840), pages 953-956, June.
    8. Adam Kepecs & Gordon Fishell, 2014. "Interneuron cell types are fit to function," Nature, Nature, vol. 505(7483), pages 318-326, January.
    9. Masayuki Matsumoto & Okihide Hikosaka, 2009. "Two types of dopamine neuron distinctly convey positive and negative motivational signals," Nature, Nature, vol. 459(7248), pages 837-841, June.
    10. Hyun-Jae Pi & Balázs Hangya & Duda Kvitsiani & Joshua I. Sanders & Z. Josh Huang & Adam Kepecs, 2013. "Cortical interneurons that specialize in disinhibitory control," Nature, Nature, vol. 503(7477), pages 521-524, November.
    11. Mattia Rigotti & Omri Barak & Melissa R. Warden & Xiao-Jing Wang & Nathaniel D. Daw & Earl K. Miller & Stefano Fusi, 2013. "The importance of mixed selectivity in complex cognitive tasks," Nature, Nature, vol. 497(7451), pages 585-590, May.
    12. Nathan R. Wilson & Caroline A. Runyan & Forea L. Wang & Mriganka Sur, 2012. "Division and subtraction by distinct cortical inhibitory networks in vivo," Nature, Nature, vol. 488(7411), pages 343-348, August.
    13. Mark M. Churchland & John P. Cunningham & Matthew T. Kaufman & Justin D. Foster & Paul Nuyujukian & Stephen I. Ryu & Krishna V. Shenoy, 2012. "Neural population dynamics during reaching," Nature, Nature, vol. 487(7405), pages 51-56, July.
    14. Nicholas A. Steinmetz & Peter Zatka-Haas & Matteo Carandini & Kenneth D. Harris, 2019. "Distributed coding of choice, action and engagement across the mouse brain," Nature, Nature, vol. 576(7786), pages 266-273, December.
    15. Guangyu Robert Yang & John D. Murray & Xiao-Jing Wang, 2016. "A dendritic disinhibitory circuit mechanism for pathway-specific gating," Nature Communications, Nature, vol. 7(1), pages 1-14, November.
    16. Joseph Cichon & Wen-Biao Gan, 2015. "Branch-specific dendritic Ca2+ spikes cause persistent synaptic plasticity," Nature, Nature, vol. 520(7546), pages 180-185, April.
    17. Zengcai V. Guo & Hidehiko K. Inagaki & Kayvon Daie & Shaul Druckmann & Charles R. Gerfen & Karel Svoboda, 2017. "Maintenance of persistent activity in a frontal thalamocortical loop," Nature, Nature, vol. 545(7653), pages 181-186, May.
    18. Ranulfo Romo & Carlos D. Brody & Adrián Hernández & Luis Lemus, 1999. "Neuronal correlates of parametric working memory in the prefrontal cortex," Nature, Nature, vol. 399(6735), pages 470-473, 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. Pierre O. Boucher & Tian Wang & Laura Carceroni & Gary Kane & Krishna V. Shenoy & Chandramouli Chandrasekaran, 2023. "Initial conditions combine with sensory evidence to induce decision-related dynamics in premotor cortex," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    2. Benjamin R Cowley & Matthew A Smith & Adam Kohn & Byron M Yu, 2016. "Stimulus-Driven Population Activity Patterns in Macaque Primary Visual Cortex," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-31, December.
    3. Arno Onken & Jue Xie & Stefano Panzeri & Camillo Padoa-Schioppa, 2019. "Categorical encoding of decision variables in orbitofrontal cortex," PLOS Computational Biology, Public Library of Science, vol. 15(10), pages 1-27, October.
    4. Ege Altan & Sara A Solla & Lee E Miller & Eric J Perreault, 2021. "Estimating the dimensionality of the manifold underlying multi-electrode neural recordings," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-23, November.
    5. Chris. I. De Zeeuw & Julius Koppen & George. G. Bregman & Marit Runge & Devika Narain, 2023. "Heterogeneous encoding of temporal stimuli in the cerebellar cortex," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    6. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Kaushik J. Lakshminarasimhan & Eric Avila & Xaq Pitkow & Dora E. Angelaki, 2023. "Dynamical latent state computation in the male macaque posterior parietal cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    8. Jan Weber & Anne-Kristin Solbakk & Alejandro O. Blenkmann & Anais Llorens & Ingrid Funderud & Sabine Leske & Pål Gunnar Larsson & Jugoslav Ivanovic & Robert T. Knight & Tor Endestad & Randolph F. Helf, 2024. "Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    9. Alireza Saeedi & Kun Wang & Ghazaleh Nikpourian & Andreas Bartels & Nikos K. Logothetis & Nelson K. Totah & Masataka Watanabe, 2024. "Brightness illusions drive a neuronal response in the primary visual cortex under top-down modulation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Wenyi Zhang & Yang Xie & Tianming Yang, 2022. "Reward salience but not spatial attention dominates the value representation in the orbitofrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    11. Hagai Lalazar & L F Abbott & Eilon Vaadia, 2016. "Tuning Curves for Arm Posture Control in Motor Cortex Are Consistent with Random Connectivity," PLOS Computational Biology, Public Library of Science, vol. 12(5), pages 1-27, May.
    12. Tristan G. Heintz & Antonio J. Hinojosa & Sina E. Dominiak & Leon Lagnado, 2022. "Opposite forms of adaptation in mouse visual cortex are controlled by distinct inhibitory microcircuits," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Katarzyna Jurewicz & Brianna J. Sleezer & Priyanka S. Mehta & Benjamin Y. Hayden & R. Becket Ebitz, 2024. "Irrational choices via a curvilinear representational geometry for value," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    14. Noel Federman & Sebastián A. Romano & Macarena Amigo-Duran & Lucca Salomon & Antonia Marin-Burgin, 2024. "Acquisition of non-olfactory encoding improves odour discrimination in olfactory cortex," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    15. Daniel Durstewitz, 2017. "A state space approach for piecewise-linear recurrent neural networks for identifying computational dynamics from neural measurements," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-33, June.
    16. João D. Semedo & Anna I. Jasper & Amin Zandvakili & Aravind Krishna & Amir Aschner & Christian K. Machens & Adam Kohn & Byron M. Yu, 2022. "Feedforward and feedback interactions between visual cortical areas use different population activity patterns," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    17. David Kappel & Bernhard Nessler & Wolfgang Maass, 2014. "STDP Installs in Winner-Take-All Circuits an Online Approximation to Hidden Markov Model Learning," PLOS Computational Biology, Public Library of Science, vol. 10(3), pages 1-22, March.
    18. Laura E. Suárez & Agoston Mihalik & Filip Milisav & Kenji Marshall & Mingze Li & Petra E. Vértes & Guillaume Lajoie & Bratislav Misic, 2024. "Connectome-based reservoir computing with the conn2res toolbox," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    19. Márton Albert Hajnal & Duy Tran & Zsombor Szabó & Andrea Albert & Karen Safaryan & Michael Einstein & Mauricio Vallejo Martelo & Pierre-Olivier Polack & Peyman Golshani & Gergő Orbán, 2024. "Shifts in attention drive context-dependent subspace encoding in anterior cingulate cortex in mice during decision making," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    20. Francesco Ceccarelli & Lorenzo Ferrucci & Fabrizio Londei & Surabhi Ramawat & Emiliano Brunamonti & Aldo Genovesio, 2023. "Static and dynamic coding in distinct cell types during associative learning in the prefrontal cortex," 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:15:y:2024:i:1:d:10.1038_s41467-024-50501-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.