IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28552-w.html
   My bibliography  Save this article

Feedforward and feedback interactions between visual cortical areas use different population activity patterns

Author

Listed:
  • João D. Semedo

    (Carnegie Mellon University)

  • Anna I. Jasper

    (Albert Einstein College of Medicine)

  • Amin Zandvakili

    (Albert Einstein College of Medicine)

  • Aravind Krishna

    (Albert Einstein College of Medicine)

  • Amir Aschner

    (Albert Einstein College of Medicine)

  • Christian K. Machens

    (Champalimaud Foundation)

  • Adam Kohn

    (Albert Einstein College of Medicine
    Albert Einstein College of Medicine
    Albert Einstein College of Medicine)

  • Byron M. Yu

    (Carnegie Mellon University
    Carnegie Mellon University)

Abstract

Brain function relies on the coordination of activity across multiple, recurrently connected brain areas. For instance, sensory information encoded in early sensory areas is relayed to, and further processed by, higher cortical areas and then fed back. However, the way in which feedforward and feedback signaling interact with one another is incompletely understood. Here we investigate this question by leveraging simultaneous neuronal population recordings in early and midlevel visual areas (V1–V2 and V1–V4). Using a dimensionality reduction approach, we find that population interactions are feedforward-dominated shortly after stimulus onset and feedback-dominated during spontaneous activity. The population activity patterns most correlated across areas were distinct during feedforward- and feedback-dominated periods. These results suggest that feedforward and feedback signaling rely on separate “channels”, which allows feedback signals to not directly affect activity that is fed forward.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28552-w
    DOI: 10.1038/s41467-022-28552-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28552-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-28552-w?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. 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.
    2. Kenneth D. Harris & Thomas D. Mrsic-Flogel, 2013. "Cortical connectivity and sensory coding," Nature, Nature, vol. 503(7474), pages 51-58, November.
    3. 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.
    4. Nuo Li & Kayvon Daie & Karel Svoboda & Shaul Druckmann, 2016. "Correction: Corrigendum: Robust neuronal dynamics in premotor cortex during motor planning," Nature, Nature, vol. 537(7618), pages 122-122, September.
    5. Hendrikje Nienborg & Bruce G. Cumming, 2009. "Decision-related activity in sensory neurons reflects more than a neuron’s causal effect," Nature, Nature, vol. 459(7243), pages 89-92, May.
    6. T. L. Veuthey & K. Derosier & S. Kondapavulur & K. Ganguly, 2020. "Single-trial cross-area neural population dynamics during long-term skill learning," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    7. Nuo Li & Kayvon Daie & Karel Svoboda & Shaul Druckmann, 2016. "Robust neuronal dynamics in premotor cortex during motor planning," Nature, Nature, vol. 532(7600), pages 459-464, 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. 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.
    2. Sara Borgomaneri & Marco Zanon & Paolo Di Luzio & Antonio Cataneo & Giorgio Arcara & Vincenzo Romei & Marco Tamietto & Alessio Avenanti, 2023. "Increasing associative plasticity in temporo-occipital back-projections improves visual perception of emotions," Nature Communications, Nature, vol. 14(1), pages 1-15, 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. Christopher F. Angeloni & Wiktor Młynarski & Eugenio Piasini & Aaron M. Williams & Katherine C. Wood & Linda Garami & Ann M. Hermundstad & Maria N. Geffen, 2023. "Dynamics of cortical contrast adaptation predict perception of signals in noise," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Alyse Thomas & Weiguo Yang & Catherine Wang & Sri Laasya Tipparaju & Guang Chen & Brennan Sullivan & Kylie Swiekatowski & Mahima Tatam & Charles Gerfen & Nuo Li, 2023. "Superior colliculus bidirectionally modulates choice activity in frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    3. Huee Ru Chong & Yadollah Ranjbar-Slamloo & Malcolm Zheng Hao Ho & Xuan Ouyang & Tsukasa Kamigaki, 2023. "Functional alterations of the prefrontal circuit underlying cognitive aging in mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. 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.
    5. 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.
    6. J. Tyler Boyd-Meredith & Alex T. Piet & Emily Jane Dennis & Ahmed El Hady & Carlos D. Brody, 2022. "Stable choice coding in rat frontal orienting fields across model-predicted changes of mind," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Tanner C Dixon & Christina M Merrick & Joni D Wallis & Richard B Ivry & Jose M Carmena, 2021. "Hybrid dedicated and distributed coding in PMd/M1 provides separation and interaction of bilateral arm signals," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-35, November.
    8. Lloyd E. Russell & Mehmet Fişek & Zidan Yang & Lynn Pei Tan & Adam M. Packer & Henry W. P. Dalgleish & Selmaan N. Chettih & Christopher D. Harvey & Michael Häusser, 2024. "The influence of cortical activity on perception depends on behavioral state and sensory context," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    9. Ryan C Williamson & Benjamin R Cowley & Ashok Litwin-Kumar & Brent Doiron & Adam Kohn & Matthew A Smith & Byron M Yu, 2016. "Scaling Properties of Dimensionality Reduction for Neural Populations and Network Models," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-27, December.
    10. Xin Wei Chia & Jian Kwang Tan & Lee Fang Ang & Tsukasa Kamigaki & Hiroshi Makino, 2023. "Emergence of cortical network motifs for short-term memory during learning," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    11. Matthijs N. Oude Lohuis & Jean L. Pie & Pietro Marchesi & Jorrit S. Montijn & Christiaan P. J. Kock & Cyriel M. A. Pennartz & Umberto Olcese, 2022. "Multisensory task demands temporally extend the causal requirement for visual cortex in perception," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    12. Bettina Voelcker & Ravi Pancholi & Simon Peron, 2022. "Transformation of primary sensory cortical representations from layer 4 to layer 2," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    13. Hannah Muysers & Hung-Ling Chen & Johannes Hahn & Shani Folschweiller & Torfi Sigurdsson & Jonas-Frederic Sauer & Marlene Bartos, 2024. "A persistent prefrontal reference frame across time and task rules," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Kaushik J Lakshminarasimhan & Alexandre Pouget & Gregory C DeAngelis & Dora E Angelaki & Xaq Pitkow, 2018. "Inferring decoding strategies for multiple correlated neural populations," PLOS Computational Biology, Public Library of Science, vol. 14(9), pages 1-40, September.
    15. Evan S. Schaffer & Neeli Mishra & Matthew R. Whiteway & Wenze Li & Michelle B. Vancura & Jason Freedman & Kripa B. Patel & Venkatakaushik Voleti & Liam Paninski & Elizabeth M. C. Hillman & L. F. Abbot, 2023. "The spatial and temporal structure of neural activity across the fly brain," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Aniruddha Das & Sarah Holden & Julie Borovicka & Jacob Icardi & Abigail O’Niel & Ariel Chaklai & Davina Patel & Rushik Patel & Stefanie Kaech Petrie & Jacob Raber & Hod Dana, 2023. "Large-scale recording of neuronal activity in freely-moving mice at cellular resolution," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    17. Georgia Koppe & Hazem Toutounji & Peter Kirsch & Stefanie Lis & Daniel Durstewitz, 2019. "Identifying nonlinear dynamical systems via generative recurrent neural networks with applications to fMRI," PLOS Computational Biology, Public Library of Science, vol. 15(8), pages 1-35, August.
    18. Andrew M. Clark & David C. Bradley, 2022. "A neural correlate of perceptual segmentation in macaque middle temporal cortical area," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    19. 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.
    20. 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.

    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_s41467-022-28552-w. 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.