Temporal integration is a robust feature of perceptual decisions
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
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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Further reading
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When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- Neuroscience
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.