IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-54700-5.html
   My bibliography  Save this article

Models optimized for real-world tasks reveal the task-dependent necessity of precise temporal coding in hearing

Author

Listed:
  • Mark R. Saddler

    (MIT
    MIT
    MIT)

  • Josh H. McDermott

    (MIT
    MIT
    MIT
    Harvard)

Abstract

Neurons encode information in the timing of their spikes in addition to their firing rates. Spike timing is particularly precise in the auditory nerve, where action potentials phase lock to sound with sub-millisecond precision, but its behavioral relevance remains uncertain. We optimized machine learning models to perform real-world hearing tasks with simulated cochlear input, assessing the precision of auditory nerve spike timing needed to reproduce human behavior. Models with high-fidelity phase locking exhibited more human-like sound localization and speech perception than models without, consistent with an essential role in human hearing. However, the temporal precision needed to reproduce human-like behavior varied across tasks, as did the precision that benefited real-world task performance. These effects suggest that perceptual domains incorporate phase locking to different extents depending on the demands of real-world hearing. The results illustrate how optimizing models for realistic tasks can clarify the role of candidate neural codes in perception.

Suggested Citation

  • Mark R. Saddler & Josh H. McDermott, 2024. "Models optimized for real-world tasks reveal the task-dependent necessity of precise temporal coding in hearing," Nature Communications, Nature, vol. 15(1), pages 1-29, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54700-5
    DOI: 10.1038/s41467-024-54700-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-54700-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-54700-5?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 Francl & Josh H. McDermott, 2022. "Author Correction: Deep neural network models of sound localization reveal how perception is adapted to real-world environments," Nature Human Behaviour, Nature, vol. 6(12), pages 1743-1744, December.
    2. Sara Popham & Dana Boebinger & Dan P. W. Ellis & Hideki Kawahara & Josh H. McDermott, 2018. "Inharmonic speech reveals the role of harmonicity in the cocktail party problem," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    3. 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.
    4. Mark R. Saddler & Ray Gonzalez & Josh H. McDermott, 2021. "Deep neural network models reveal interplay of peripheral coding and stimulus statistics in pitch perception," Nature Communications, Nature, vol. 12(1), pages 1-25, December.
    5. Richard McWalter & Josh H. McDermott, 2019. "Illusory sound texture reveals multi-second statistical completion in auditory scene analysis," Nature Communications, Nature, vol. 10(1), pages 1-18, December.
    6. Alexander J. E. Kell & Josh H. McDermott, 2019. "Invariance to background noise as a signature of non-primary auditory cortex," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    7. Nicol S. Harper & David McAlpine, 2004. "Optimal neural population coding of an auditory spatial cue," Nature, Nature, vol. 430(7000), pages 682-686, August.
    8. Andrew Francl & Josh H. McDermott, 2022. "Deep neural network models of sound localization reveal how perception is adapted to real-world environments," Nature Human Behaviour, Nature, vol. 6(1), pages 111-133, January.
    9. Malinda J. McPherson & Josh H. McDermott, 2018. "Diversity in pitch perception revealed by task dependence," Nature Human Behaviour, Nature, vol. 2(1), pages 52-66, January.
    10. Abhijit Kulkarni & H. Steven Colburn, 1998. "Role of spectral detail in sound-source localization," Nature, Nature, vol. 396(6713), pages 747-749, December.
    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. Liu, Yang & Pedrycz, Witold & Deveci, Muhammet & Chen, Zhen-Song, 2024. "BIM-based building performance assessment of green buildings - A case study from China," Applied Energy, Elsevier, vol. 373(C).
    2. Ariel Goldstein & Avigail Grinstein-Dabush & Mariano Schain & Haocheng Wang & Zhuoqiao Hong & Bobbi Aubrey & Samuel A. Nastase & Zaid Zada & Eric Ham & Amir Feder & Harshvardhan Gazula & Eliav Buchnik, 2024. "Alignment of brain embeddings and artificial contextual embeddings in natural language points to common geometric patterns," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Simon Weiler & Vahid Rahmati & Marcel Isstas & Johann Wutke & Andreas Walter Stark & Christian Franke & Jürgen Graf & Christian Geis & Otto W. Witte & Mark Hübener & Jürgen Bolz & Troy W. Margrie & Kn, 2024. "A primary sensory cortical interareal feedforward inhibitory circuit for tacto-visual integration," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    4. Catarina Mendonça & Pietro Mandelli & Ville Pulkki, 2016. "Modeling the Perception of Audiovisual Distance: Bayesian Causal Inference and Other Models," PLOS ONE, Public Library of Science, vol. 11(12), pages 1-18, December.
    5. Jacques Pesnot Lerousseau & Cesare V. Parise & Marc O. Ernst & Virginie Wassenhove, 2022. "Multisensory correlation computations in the human brain identified by a time-resolved encoding model," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    6. Mark R. Saddler & Ray Gonzalez & Josh H. McDermott, 2021. "Deep neural network models reveal interplay of peripheral coding and stimulus statistics in pitch perception," Nature Communications, Nature, vol. 12(1), pages 1-25, 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. Marine Hainguerlot & Thibault Gajdos & Jean-Christophe Vergnaud & Vincent de Gardelle, 2023. "How Overconfidence Bias Influences Suboptimality in Perceptual Decision Making," PSE-Ecole d'économie de Paris (Postprint) hal-04197403, HAL.
    9. 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.
    10. Patricia Besson & Christophe Bourdin & Lionel Bringoux, 2011. "A Comprehensive Model of Audiovisual Perception: Both Percept and Temporal Dynamics," PLOS ONE, Public Library of Science, vol. 6(8), pages 1-11, August.
    11. 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.
    12. 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.
    13. Wendy J Adams, 2016. "The Development of Audio-Visual Integration for Temporal Judgements," PLOS Computational Biology, Public Library of Science, vol. 12(4), pages 1-17, April.
    14. 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.
    15. Xiaochen Zhang & Lingling Jin & Jie Zhao & Jiazhen Li & Ding-Bang Luh & Tiansheng Xia, 2022. "The Influences of Different Sensory Modalities and Cognitive Loads on Walking Navigation: A Preliminary Study," Sustainability, MDPI, vol. 14(24), pages 1-14, December.
    16. Johannes Burge & Priyank Jaini, 2017. "Accuracy Maximization Analysis for Sensory-Perceptual Tasks: Computational Improvements, Filter Robustness, and Coding Advantages for Scaled Additive Noise," PLOS Computational Biology, Public Library of Science, vol. 13(2), pages 1-32, February.
    17. Yingjie Lai & Chaemoon Yoo & Xiaomin Zhou & Younghwan Pan, 2023. "Elements of Food Service Design for Low-Carbon Tourism-Based on Dine-In Tourist Behavior and Attitudes in China," Sustainability, MDPI, vol. 15(9), pages 1-21, May.
    18. Florent Meyniel & Maxime Maheu & Stanislas Dehaene, 2016. "Human Inferences about Sequences: A Minimal Transition Probability Model," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-26, December.
    19. 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.
    20. Jean-François Patri & Pascal Perrier & Jean-Luc Schwartz & Julien Diard, 2018. "What drives the perceptual change resulting from speech motor adaptation? Evaluation of hypotheses in a Bayesian modeling framework," PLOS Computational Biology, Public Library of Science, vol. 14(1), pages 1-38, January.

    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_s41467-024-54700-5. 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.