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          Abstract

          Humans have been shown to adapt to the temporal statistics of timing tasks so as to optimize the accuracy of their responses, in agreement with the predictions of Bayesian integration. This suggests that they build an internal representation of both the experimentally imposed distribution of time intervals (the prior) and of the error (the loss function). The responses of a Bayesian ideal observer depend crucially on these internal representations, which have only been previously studied for simple distributions. To study the nature of these representations we asked subjects to reproduce time intervals drawn from underlying temporal distributions of varying complexity, from uniform to highly skewed or bimodal while also varying the error mapping that determined the performance feedback. Interval reproduction times were affected by both the distribution and feedback, in good agreement with a performance-optimizing Bayesian observer and actor model. Bayesian model comparison highlighted that subjects were integrating the provided feedback and represented the experimental distribution with a smoothed approximation. A nonparametric reconstruction of the subjective priors from the data shows that they are generally in agreement with the true distributions up to third-order moments, but with systematically heavier tails. In particular, higher-order statistical features (kurtosis, multimodality) seem much harder to acquire. Our findings suggest that humans have only minor constraints on learning lower-order statistical properties of unimodal (including peaked and skewed) distributions of time intervals under the guidance of corrective feedback, and that their behavior is well explained by Bayesian decision theory.

          Author Summary

          Human performance in a timing task depends on the context of recently experienced time intervals. In fact, people may use prior experience to improve their timing performance. Given the relevance of time for both sensing and acting in the world, how humans learn and represent temporal information is a fundamental question in neuroscience. Here, we ask subjects to reproduce the duration of time intervals drawn from different distributions (different temporal contexts). We build a set of models of how people might behave in such a timing task, depending on how they are representing the temporal context. Comparison between models and data allows us to establish that in general subjects are integrating task-relevant temporal information with the provided error feedback to enhance their timing performance. Analysis of the subjects' responses allows us to reconstruct their internal representation of the temporal context, and we compare it with the true distribution. We find that with the help of corrective feedback humans can learn good approximations of unimodal distributions of time intervals used in the experiment, even for skewed distributions of durations; on the other hand, under similar conditions, we find that multimodal distributions of timing intervals are much harder to acquire.

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          Most cited references51

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          What makes us tick? Functional and neural mechanisms of interval timing.

          Time is a fundamental dimension of life. It is crucial for decisions about quantity, speed of movement and rate of return, as well as for motor control in walking, speech, playing or appreciating music, and participating in sports. Traditionally, the way in which time is perceived, represented and estimated has been explained using a pacemaker-accumulator model that is not only straightforward, but also surprisingly powerful in explaining behavioural and biological data. However, recent advances have challenged this traditional view. It is now proposed that the brain represents time in a distributed manner and tells the time by detecting the coincidental activation of different neural populations.
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            Bayesian integration in sensorimotor learning.

            When we learn a new motor skill, such as playing an approaching tennis ball, both our sensors and the task possess variability. Our sensors provide imperfect information about the ball's velocity, so we can only estimate it. Combining information from multiple modalities can reduce the error in this estimate. On a longer time scale, not all velocities are a priori equally probable, and over the course of a match there will be a probability distribution of velocities. According to bayesian theory, an optimal estimate results from combining information about the distribution of velocities-the prior-with evidence from sensory feedback. As uncertainty increases, when playing in fog or at dusk, the system should increasingly rely on prior knowledge. To use a bayesian strategy, the brain would need to represent the prior distribution and the level of uncertainty in the sensory feedback. Here we control the statistical variations of a new sensorimotor task and manipulate the uncertainty of the sensory feedback. We show that subjects internally represent both the statistical distribution of the task and their sensory uncertainty, combining them in a manner consistent with a performance-optimizing bayesian process. The central nervous system therefore employs probabilistic models during sensorimotor learning.
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              The ventriloquist effect results from near-optimal bimodal integration.

              Ventriloquism is the ancient art of making one's voice appear to come from elsewhere, an art exploited by the Greek and Roman oracles, and possibly earlier. We regularly experience the effect when watching television and movies, where the voices seem to emanate from the actors' lips rather than from the actual sound source. Originally, ventriloquism was explained by performers projecting sound to their puppets by special techniques, but more recently it is assumed that ventriloquism results from vision "capturing" sound. In this study we investigate spatial localization of audio-visual stimuli. When visual localization is good, vision does indeed dominate and capture sound. However, for severely blurred visual stimuli (that are poorly localized), the reverse holds: sound captures vision. For less blurred stimuli, neither sense dominates and perception follows the mean position. Precision of bimodal localization is usually better than either the visual or the auditory unimodal presentation. All the results are well explained not by one sense capturing the other, but by a simple model of optimal combination of visual and auditory information.
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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
                November 2012
                November 2012
                29 November 2012
                : 8
                : 11
                : e1002771
                Affiliations
                [1 ]Institute of Perception, Action and Behaviour, School of Informatics, University of Edinburgh, Edinburgh, United Kingdom
                [2 ]Doctoral Training Centre in Neuroinformatics and Computational Neuroscience, School of Informatics, University of Edinburgh, Edinburgh, United Kingdom
                [3 ]Computational and Biological Learning Lab, Department of Engineering, University of Cambridge, Cambridge, United Kingdom
                New York University, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LA DMW SV. Performed the experiments: LA. Analyzed the data: LA. Wrote the paper: LA DMW SV.

                Article
                PCOMPBIOL-D-12-00860
                10.1371/journal.pcbi.1002771
                3510049
                23209386
                34d79a6c-c07e-43d3-a626-a47dd7f649ec
                Copyright @ 2012

                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
                : 25 May 2012
                : 24 September 2012
                Page count
                Pages: 19
                Funding
                This study was supported by an Engineering and Physical Sciences Research Council/Medical Research Council scholarship granted to LA from the Neuroinformatics and Computational Neuroscience Doctoral Training Centre at the University of Edinburgh. DMW is supported by the Wellcome Trust and the Human Frontiers Science Program. SV is supported through grants from Microsoft Research, Royal Academy of Engineering and EU FP7 programs. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Neuroscience
                Sensory Perception
                Psychophysics
                Computational Neuroscience
                Motor Systems

                Quantitative & Systems biology
                Quantitative & Systems biology

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