IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29457-4.html
   My bibliography  Save this article

Neural structure of a sensory decoder for motor control

Author

Listed:
  • Seth W. Egger

    (Duke University School of Medicine)

  • Stephen G. Lisberger

    (Duke University School of Medicine)

Abstract

The transformation of sensory input to motor output is often conceived as a decoder operating on neural representations. We seek a mechanistic understanding of sensory decoding by mimicking neural circuitry in the decoder’s design. The results of a simple experiment shape our approach. Changing the size of a target for smooth pursuit eye movements changes the relationship between the variance and mean of the evoked behavior in a way that contradicts the regime of “signal-dependent noise” and defies traditional decoding approaches. A theoretical analysis leads us to propose a circuit for pursuit that includes multiple parallel pathways and multiple sources of variation. Behavioral and neural responses with biomimetic statistics emerge from a biologically-motivated circuit model with noise in the pathway that is dedicated to flexibly adjusting the strength of visual-motor transmission. Our results demonstrate the power of re-imagining decoding as processing through the parallel pathways of neural systems.

Suggested Citation

  • Seth W. Egger & Stephen G. Lisberger, 2022. "Neural structure of a sensory decoder for motor control," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29457-4
    DOI: 10.1038/s41467-022-29457-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29457-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-29457-4?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. Evan D. Remington & Tiffany V. Parks & Mehrdad Jazayeri, 2018. "Late Bayesian inference in mental transformations," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    2. Marc O. Ernst & Martin S. Banks, 2002. "Humans integrate visual and haptic information in a statistically optimal fashion," Nature, Nature, vol. 415(6870), pages 429-433, January.
    3. Mehrdad Jazayeri & J. Anthony Movshon, 2007. "A new perceptual illusion reveals mechanisms of sensory decoding," Nature, Nature, vol. 446(7138), pages 912-915, April.
    4. Masaki Tanaka & Stephen G. Lisberger, 2001. "Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex," Nature, Nature, vol. 409(6817), pages 191-194, January.
    5. Christopher M. Harris & Daniel M. Wolpert, 1998. "Signal-dependent noise determines motor planning," Nature, Nature, vol. 394(6695), pages 780-784, August.
    6. Luigi Acerbi & Sethu Vijayakumar & Daniel M Wolpert, 2014. "On the Origins of Suboptimality in Human Probabilistic Inference," PLOS Computational Biology, Public Library of Science, vol. 10(6), pages 1-23, June.
    7. Leslie C. Osborne & Stephen G. Lisberger & William Bialek, 2005. "A sensory source for motor variation," Nature, Nature, vol. 437(7057), pages 412-416, September.
    8. Konrad P. Körding & Daniel M. Wolpert, 2004. "Bayesian integration in sensorimotor learning," Nature, Nature, vol. 427(6971), pages 244-247, January.
    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. Adam N Sanborn & Ulrik R Beierholm, 2016. "Fast and Accurate Learning When Making Discrete Numerical Estimates," PLOS Computational Biology, Public Library of Science, vol. 12(4), pages 1-28, April.
    2. Tim Genewein & Eduard Hez & Zeynab Razzaghpanah & Daniel A Braun, 2015. "Structure Learning in Bayesian Sensorimotor Integration," PLOS Computational Biology, Public Library of Science, vol. 11(8), pages 1-27, August.
    3. Jonathan B Dingwell & Joby John & Joseph P Cusumano, 2010. "Do Humans Optimally Exploit Redundancy to Control Step Variability in Walking?," PLOS Computational Biology, Public Library of Science, vol. 6(7), pages 1-15, July.
    4. Jingwei Sun & Jian Li & Hang Zhang, 2019. "Human representation of multimodal distributions as clusters of samples," PLOS Computational Biology, Public Library of Science, vol. 15(5), pages 1-29, May.
    5. Kang He & You Liang & Farnaz Abdollahi & Moria Fisher Bittmann & Konrad Kording & Kunlin Wei, 2016. "The Statistical Determinants of the Speed of Motor Learning," PLOS Computational Biology, Public Library of Science, vol. 12(9), pages 1-20, September.
    6. Shih-Wei Wu & Maria F Dal Martello & Laurence T Maloney, 2009. "Sub-Optimal Allocation of Time in Sequential Movements," PLOS ONE, Public Library of Science, vol. 4(12), pages 1-13, December.
    7. 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.
    8. Caroline Haimerl & Douglas A. Ruff & Marlene R. Cohen & Cristina Savin & Eero P. Simoncelli, 2023. "Targeted V1 comodulation supports task-adaptive sensory decisions," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Brocas, Isabelle & Carrillo, Juan D., 2012. "From perception to action: An economic model of brain processes," Games and Economic Behavior, Elsevier, vol. 75(1), pages 81-103.
    10. Carrillo, Juan & Brocas, Isabelle, 2007. "Reason, Emotion and Information Processing in the Brain," CEPR Discussion Papers 6535, C.E.P.R. Discussion Papers.
    11. Jannes Jegminat & Maya A Jastrzębowska & Matthew V Pachai & Michael H Herzog & Jean-Pascal Pfister, 2020. "Bayesian regression explains how human participants handle parameter uncertainty," PLOS Computational Biology, Public Library of Science, vol. 16(5), pages 1-23, May.
    12. Elina Stengård & Ronald van den Berg, 2019. "Imperfect Bayesian inference in visual perception," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-27, April.
    13. Vassilios N Christopoulos & Paul R Schrater, 2009. "Grasping Objects with Environmentally Induced Position Uncertainty," PLOS Computational Biology, Public Library of Science, vol. 5(10), pages 1-11, October.
    14. Guido Marco Cicchini & Giovanni D’Errico & David Charles Burr, 2022. "Crowding results from optimal integration of visual targets with contextual information," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    15. Long Luu & Alan A Stocker, 2021. "Categorical judgments do not modify sensory representations in working memory," PLOS Computational Biology, Public Library of Science, vol. 17(6), pages 1-28, June.
    16. Udo A Ernst & Sunita Mandon & Nadja Schinkel–Bielefeld & Simon D Neitzel & Andreas K Kreiter & Klaus R Pawelzik, 2012. "Optimality of Human Contour Integration," PLOS Computational Biology, Public Library of Science, vol. 8(5), pages 1-17, May.
    17. Philipp Schustek & Rubén Moreno-Bote, 2018. "Instance-based generalization for human judgments about uncertainty," PLOS Computational Biology, Public Library of Science, vol. 14(6), pages 1-27, June.
    18. Ian H Stevenson & Hugo L Fernandes & Iris Vilares & Kunlin Wei & Konrad P Körding, 2009. "Bayesian Integration and Non-Linear Feedback Control in a Full-Body Motor Task," PLOS Computational Biology, Public Library of Science, vol. 5(12), pages 1-9, December.
    19. Luigi Acerbi & Kalpana Dokka & Dora E Angelaki & Wei Ji Ma, 2018. "Bayesian comparison of explicit and implicit causal inference strategies in multisensory heading perception," PLOS Computational Biology, Public Library of Science, vol. 14(7), pages 1-38, July.
    20. Paolo Tommasino & Antonella Maselli & Domenico Campolo & Francesco Lacquaniti & Andrea d’Avella, 2021. "A Hessian-based decomposition characterizes how performance in complex motor skills depends on individual strategy and variability," PLOS ONE, Public Library of Science, vol. 16(6), pages 1-32, June.

    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_s41467-022-29457-4. 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.