1. Neuroscience

Temporal integration is a robust feature of perceptual decisions

  1. Alexandre Hyafil  Is a corresponding author
  2. Jaime de la Rocha
  3. Cristina Pericas
  4. Leor N Katz
  5. Alexander C Huk
  6. Jonathan W Pillow
  1. Centre de Recerca Matemàtica, Spain
  2. Institut d'Investigacions Biomèdiques August Pi i Sunyer, Spain
  3. National Eye Institute, United States
  4. University of California, Los Angeles, United States
  5. Princeton University, United States
https://doi.org/10.7554/eLife.84045
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  1. Alexandre Hyafil
  2. Jaime de la Rocha
  3. Cristina Pericas
  4. Leor N Katz
  5. Alexander C Huk
  6. Jonathan W Pillow
(2023)
Temporal integration is a robust feature of perceptual decisions
eLife 12:e84045.
https://doi.org/10.7554/eLife.84045
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Abstract

Making informed decisions in noisy environments requires integrating sensory information over time. However, recent work has suggested that it may be difficult to determine whether an animal's decision-making strategy relies on evidence integration or not. In particular, strategies based on extrema-detection or random snapshots of the evidence stream may be difficult or even impossible to distinguish from classic evidence integration. Moreover, such non-integration strategies might be surprisingly common in experiments that aimed to study decisions based on integration. To determine whether temporal integration is central to perceptual decision making, we developed a new model-based approach for comparing temporal integration against alternative 'non-integration' strategies for tasks in which the sensory signal is composed of discrete stimulus samples. We applied these methods to behavioral data from monkeys, rats, and humans performing a variety of sensory decision-making tasks. In all species and tasks, we found converging evidence in favor of temporal integration. First, in all observers across studies, the integration model better accounted for standard behavioral statistics such as psychometric curves and psychophysical kernels. Second, we found that sensory samples with large evidence do not contribute disproportionately to subject choices, as predicted by an extrema-detection strategy. Finally, we provide a direct confirmation of temporal integration by showing that the sum of both early and late evidence contributed to observer decisions. Overall, our results provide experimental evidence suggesting that temporal integration is an ubiquitous feature in mammalian perceptual decision-making. Our study also highlights the benefits of using experimental paradigms where the temporal stream of sensory evidence is controlled explicitly by the experimenter, and known precisely by the analyst, to characterize the temporal properties of the decision process.

Data availability

All experimental data (behavioral and neural data in monkeys, behavioral data in rats and humans) and code to run the analysis are publicly available at https://github.com/ahyafil/TemporalIntegration.

Article and author information

Author details

  1. Alexandre Hyafil

    Centre de Recerca Matemàtica, Bellaterra, Spain
    For correspondence
    alexandre.hyafil@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0566-651X

  2. Jaime de la Rocha

    Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3314-9384

  3. Cristina Pericas

    Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.

  4. Leor N Katz

    Laboratory of Sensorimotor Research, National Eye Institute, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2742-6533

  5. Alexander C Huk

    Department of Psychiatry, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Jonathan W Pillow

    Department of Psychology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3638-8831

Funding

Agencia Estatal de Investigación (RYC-2017-23231)

  • Alexandre Hyafil

Ministerio de Economía y Competitividad (SAF2015-70324-R)

  • Jaime de la Rocha

European Research Council (ERC-2015-CoG-683209)

  • Jaime de la Rocha

National Institutes of Health (R01EY017366)

  • Alexander C Huk
  • Jonathan W Pillow

National Institutes of Health (NS104899)

  • Jonathan W Pillow

Simons Collaboration for the Global Brain (SCGB AWD543027)

  • Jonathan W Pillow

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Rat experiments were approved by the local ethics committee of the University of Barcelona 658 (Comité d'Experimentació Animal, Barcelona, Spain, protocol number Ref 390/14).Monkey experiment: All experimental protocols were approved by The University of Texas Institutional Animal Care and Use Committee (AUP-2012-00085, AUP-2015-00068) and in accordance with National Institute of Health standards for care and use of laboratory animals.

Human subjects: Informed consent was obtained from all participants. The experiment with human participants was approved by the UPF ethics committee (approval 654 2013/5435/I from CEIm- Parc de Salut MAR).

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Alexandre Hyafil
  2. Jaime de la Rocha
  3. Cristina Pericas
  4. Leor N Katz
  5. Alexander C Huk
  6. Jonathan W Pillow
(2023)
Temporal integration is a robust feature of perceptual decisions
eLife 12:e84045.
https://doi.org/10.7554/eLife.84045

Share this article

https://doi.org/10.7554/eLife.84045

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