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

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.

Metrics

  • 2,234
    views
  • 263
    downloads
  • 10
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Neuroscience
    Jacob A Miller
    Insight

    When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.

    1. Neuroscience
    Zhujun Shao, Mengya Zhang, Qing Yu
    Research Article

    When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.