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      How the Brain Decides When to Work and When to Rest: Dissociation of Implicit-Reactive from Explicit-Predictive Computational Processes

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      PLoS Computational Biology
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          Abstract

          A pervasive case of cost-benefit problem is how to allocate effort over time, i.e. deciding when to work and when to rest. An economic decision perspective would suggest that duration of effort is determined beforehand, depending on expected costs and benefits. However, the literature on exercise performance emphasizes that decisions are made on the fly, depending on physiological variables. Here, we propose and validate a general model of effort allocation that integrates these two views. In this model, a single variable, termed cost evidence, accumulates during effort and dissipates during rest, triggering effort cessation and resumption when reaching bounds. We assumed that such a basic mechanism could explain implicit adaptation, whereas the latent parameters (slopes and bounds) could be amenable to explicit anticipation. A series of behavioral experiments manipulating effort duration and difficulty was conducted in a total of 121 healthy humans to dissociate implicit-reactive from explicit-predictive computations. Results show 1) that effort and rest durations are adapted on the fly to variations in cost-evidence level, 2) that the cost-evidence fluctuations driving the behavior do not match explicit ratings of exhaustion, and 3) that actual difficulty impacts effort duration whereas expected difficulty impacts rest duration. Taken together, our findings suggest that cost evidence is implicitly monitored online, with an accumulation rate proportional to actual task difficulty. In contrast, cost-evidence bounds and dissipation rate might be adjusted in anticipation, depending on explicit task difficulty.

          Author Summary

          Imagine that ahead of you is a long time of work: when will you take a break? This sort of issue – how to allocate effort over time – has been addressed by distinct theoretical fields, with different emphasis on reactive and predictive processes. An intuitive view is that you start working, stop when you are tired, and start again when fatigue goes away. Biologically, this means that decisions are taken when some physiological variable reaches a given bound on the risk of homeostatic failure. In a more economic perspective, fatigue translates into effort cost, which must be anticipated and compared to expected benefit before engaging an action. We proposed a computational model that bridges these perspectives from sport physiology and decision theory. Decisions are made in reaction to bounds being reached by an implicit cost variable that accumulates during effort, at a rate proportional to task difficulty, and dissipates during rest. However, some latent parameters (bounds and dissipation rate) are adjusted in anticipation, depending on explicit costs and benefits. This model was supported by behavioral data obtained using a paradigm where participants squeeze a handgrip to win a monetary payoff proportional to effort duration.

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          Most cited references28

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          Visual fixations and the computation and comparison of value in simple choice.

          Most organisms facing a choice between multiple stimuli will look repeatedly at them, presumably implementing a comparison process between the items' values. Little is known about the nature of the comparison process in value-based decision-making or about the role of visual fixations in this process. We created a computational model of value-based binary choice in which fixations guide the comparison process and tested it on humans using eye-tracking. We found that the model can quantitatively explain complex relationships between fixation patterns and choices, as well as several fixation-driven decision biases.
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            What is the Bereitschaftspotential?

            Since discovery of the slow negative electroencephalographic (EEG) activity preceding self-initiated movement by Kornhuber and Deecke [Kornhuber HH, Deecke L. Hirnpotentialänderungen bei Willkurbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflugers Archiv 1965;284:1-17], various source localization techniques in normal subjects and epicortical recording in epilepsy patients have disclosed the generator mechanisms of each identifiable component of movement-related cortical potentials (MRCPs) to some extent. The initial slow segment of BP, called 'early BP' in this article, begins about 2 s before the movement onset in the pre-supplementary motor area (pre-SMA) with no site-specificity and in the SMA proper according to the somatotopic organization, and shortly thereafter in the lateral premotor cortex bilaterally with relatively clear somatotopy. About 400 ms before the movement onset, the steeper negative slope, called 'late BP' in this article (also referred to as NS'), occurs in the contralateral primary motor cortex (M1) and lateral premotor cortex with precise somatotopy. These two phases of BP are differentially influenced by various factors, especially by complexity of the movement which enhances only the late BP. Event-related desynchronization (ERD) of beta frequency EEG band before self-initiated movements shows a different temporospatial pattern from that of the BP, suggesting different neuronal mechanisms for the two. BP has been applied for investigating pathophysiology of various movement disorders. Volitional motor inhibition or muscle relaxation is preceded by BP quite similar to that preceding voluntary muscle contraction. Since BP of typical waveforms and temporospatial pattern does not occur before organic involuntary movements, BP is used for detecting the participation of the 'voluntary motor system' in the generation of apparently involuntary movements in patients with psychogenic movement disorders. In view of Libet et al.'s report [Libet B, Gleason CA, Wright EW, Pearl DK. Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 1983;106:623-642] that the awareness of intention to move occurred much later than the onset of BP, the early BP might reflect, physiologically, slowly increasing cortical excitability and, behaviorally, subconscious readiness for the forthcoming movement. Whether the late BP reflects conscious preparation for intended movement or not remains to be clarified.
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              The neural mechanisms of inter-temporal decision-making: understanding variability.

              Humans and animals prefer immediate over delayed rewards (delay discounting). This preference for smaller-but-sooner over larger-but-later rewards shows substantial interindividual variability in healthy subjects. Moreover, a strong bias towards immediate reinforcement characterizes many psychiatric conditions such as addiction and attention-deficit hyperactivity disorder. We discuss the neural mechanisms underlying delay discounting and describe how interindividual variability (trait effects) in the neural instantiation of subprocesses of delay discounting (such as reward valuation, cognitive control and prospection) contributes to differences in behaviour. We next discuss different interventions that can partially remedy impulsive decision-making (state effects). Although the precise neural mechanisms underlying many of these modulating influences are only beginning to be unravelled, they point towards novel treatment approaches for disorders of impulse control. Copyright © 2011 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                April 2014
                17 April 2014
                : 10
                : 4
                : e1003584
                Affiliations
                [1]Motivation, Brain & Behavior (MBB) team, Institut du Cerveau et de la Moelle épinière (ICM), Groupe Hospitalier Pitié-Salpêtrière, Université Pierre et Marie Curie (UPMC – Paris 6), Paris, France
                Oxford University, United Kingdom
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: FM LS MP. Performed the experiments: FM LS. Analyzed the data: FM LS. Wrote the paper: FM MP.

                Article
                PCOMPBIOL-D-13-01589
                10.1371/journal.pcbi.1003584
                3990494
                24743711
                b62c9a84-09cc-4392-afff-68d73d224869
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 September 2013
                : 12 March 2014
                Page count
                Pages: 16
                Funding
                The study was funded by a Starting Grant (BioMotiv) from the European Research Council to MP. This work also benefited from the “Investissements d'Avenir” program (ANR-10-IAIHU-06). FM and LS were financially supported by the French Ministère de la Recherche. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Neuroscience
                Cognitive Neuroscience
                Consciousness
                Motor Reactions
                Cognitive Science
                Cognition
                Decision Making
                Cognitive Psychology
                Motivation
                Sensory Perception
                Psychophysics
                Psychology
                Behavior
                Human Performance
                Medicine and Health Sciences
                Pain Management
                Pain
                Social Sciences

                Quantitative & Systems biology
                Quantitative & Systems biology

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