Visual attention modulates the integration of goal-relevant evidence and not value
Abstract
When choosing between options, such as food items presented in plain view, people tend to choose the option they spend longer looking at. The prevailing interpretation is that visual attention increases value. However, in previous studies, 'value' was coupled to a behavioural goal, since subjects had to choose the item they preferred. This makes it impossible to discern if visual attention has an effect on value, or, instead, if attention modulates the information most relevant for the goal of the decision-maker. Here we present the results of two independent studies—a perceptual and a value-based task—that allow us to decouple value from goal-relevant information using specific task-framing. Combining psychophysics with computational modelling, we show that, contrary to the current interpretation, attention does not boost value, but instead it modulates goal-relevant information. This work provides a novel and more general mechanism by which attention interacts with choice.
Data availability
Data and the codes used for this study have been deposited at the Brain Decision Modelling Lab GitHub (https://github.com/BDMLab).
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Sepulveda_et_al_2020GitHub repository, BDM lab Sepulveda_et_al_2020.
Article and author information
Author details
Funding
Chilean National Agency for Research and Development (Graduate student scholarship - DOCTORADO BECAS CHILE/2017 - 72180193)
- Pradyumna Sepulveda
Wellcome Trust (Sir Henry Dale Fellowship (102612 /A/13/Z))
- Benedetto De Martino
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: All participants signed a consent form and both studies were done following the approval given by the University College London, Division of Psychology and Language Sciences ethics committee (project ID number 1825/003).
Reviewing Editor
- Valentin Wyart, École normale supérieure, PSL University, INSERM, France
Publication history
- Received: July 3, 2020
- Accepted: November 16, 2020
- Accepted Manuscript published: November 17, 2020 (version 1)
- Version of Record published: December 8, 2020 (version 2)
Copyright
© 2020, Sepulveda et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Computational and Systems Biology
- Neuroscience
To decide whether a course of action is worth pursuing, individuals typically weigh its expected costs and benefits. Optimal decision-making relies upon accurate effort cost anticipation, which is generally assumed to be performed independently from goal valuation. In two experiments (n = 46), we challenged this independence principle of standard decision theory. We presented participants with a series of treadmill routes randomly associated to monetary rewards and collected both ‘accept’ versus ‘decline’ decisions and subjective estimates of energetic cost. Behavioural results show that higher monetary prospects led participants to provide higher cost estimates, although reward was independent from effort in our design. Among candidate cognitive explanations, they support a model in which prospective cost assessment is biased by the output of an automatic computation adjusting effort expenditure to goal value. This decision bias might lead people to abandon the pursuit of valuable goals that are in fact not so costly to achieve.
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- Computational and Systems Biology
- Neuroscience
Synaptic communication relies on the fusion of synaptic vesicles with the plasma membrane, which leads to neurotransmitter release. This exocytosis is triggered by brief and local elevations of intracellular Ca2+ with remarkably high sensitivity. How this is molecularly achieved is unknown. While synaptotagmins confer the Ca2+ sensitivity of neurotransmitter exocytosis, biochemical measurements reported Ca2+ affinities too low to account for synaptic function. However, synaptotagmin's Ca2+ affinity increases upon binding the plasma membrane phospholipid PI(4,5)P2 and, vice versa, Ca2+-binding increases synaptotagmin's PI(4,5)P2 affinity, indicating a stabilization of the Ca2+/PI(4,5)P2 dual-bound syt. Here we devise a molecular exocytosis model based on this positive allosteric stabilization and the assumptions that (1.) synaptotagmin Ca2+/PI(4,5)P2 dual binding lowers the energy barrier for vesicle fusion and that (2.) the effect of multiple synaptotagmins on the energy barrier is additive. The model, which relies on biochemically measured Ca2+/PI(4,5)P2 affinities and protein copy numbers, reproduced the steep Ca2+ dependency of neurotransmitter release. Our results indicate that each synaptotagmin dual binding Ca2+/PI(4,5)P2 lowers the energy barrier for vesicle fusion by ~5 kBT and that allosteric stabilization of this state enables the synchronized engagement of several (typically three) synaptotagmins for fast exocytosis. Furthermore, we show that mutations altering synaptotagmin’s allosteric properties may show dominant-negative effects, even though synaptotagmins act independently on the energy barrier, and that dynamic changes of local PI(4,5)P2 (e.g. upon vesicle movement) dramatically impact synaptic responses. We conclude that allosterically stabilized Ca2+/PI(4,5)P2 dual binding enables synaptotagmins to exert their coordinated function in neurotransmission.