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      Human visual exploration reduces uncertainty about the sensed world

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          Abstract

          In previous papers, we introduced a normative scheme for scene construction and epistemic (visual) searches based upon active inference. This scheme provides a principled account of how people decide where to look, when categorising a visual scene based on its contents. In this paper, we use active inference to explain the visual searches of normal human subjects; enabling us to answer some key questions about visual foraging and salience attribution. First, we asked whether there is any evidence for ‘epistemic foraging’; i.e. exploration that resolves uncertainty about a scene. In brief, we used Bayesian model comparison to compare Markov decision process (MDP) models of scan-paths that did–and did not–contain the epistemic, uncertainty-resolving imperatives for action selection. In the course of this model comparison, we discovered that it was necessary to include non-epistemic (heuristic) policies to explain observed behaviour (e.g., a reading-like strategy that involved scanning from left to right). Despite this use of heuristic policies, model comparison showed that there is substantial evidence for epistemic foraging in the visual exploration of even simple scenes. Second, we compared MDP models that did–and did not–allow for changes in prior expectations over successive blocks of the visual search paradigm. We found that implicit prior beliefs about the speed and accuracy of visual searches changed systematically with experience. Finally, we characterised intersubject variability in terms of subject-specific prior beliefs. Specifically, we used canonical correlation analysis to see if there were any mixtures of prior expectations that could predict between-subject differences in performance; thereby establishing a quantitative link between different behavioural phenotypes and Bayesian belief updating. We demonstrated that better scene categorisation performance is consistently associated with lower reliance on heuristics; i.e., a greater use of a generative model of the scene to direct its exploration.

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          Most cited references15

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          Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia.

          The clinical hallmark of schizophrenia is psychosis. The objective of this overview is to link the neurobiology (brain), the phenomenological experience (mind), and pharmacological aspects of psychosis-in-schizophrenia into a unitary framework. Current ideas regarding the neurobiology and phenomenology of psychosis and schizophrenia, the role of dopamine, and the mechanism of action of antipsychotic medication were integrated to develop this framework. A central role of dopamine is to mediate the "salience" of environmental events and internal representations. It is proposed that a dysregulated, hyperdopaminergic state, at a "brain" level of description and analysis, leads to an aberrant assignment of salience to the elements of one's experience, at a "mind" level. Delusions are a cognitive effort by the patient to make sense of these aberrantly salient experiences, whereas hallucinations reflect a direct experience of the aberrant salience of internal representations. Antipsychotics "dampen the salience" of these abnormal experiences and by doing so permit the resolution of symptoms. The antipsychotics do not erase the symptoms but provide the platform for a process of psychological resolution. However, if antipsychotic treatment is stopped, the dysregulated neurochemistry returns, the dormant ideas and experiences become reinvested with aberrant salience, and a relapse occurs. The article provides a heuristic framework for linking the psychological and biological in psychosis. Predictions of this hypothesis, particularly regarding the possibility of synergy between psychological and pharmacological therapies, are presented. The author describes how the hypothesis is complementary to other ideas about psychosis and also discusses its limitations.
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            Contextual cueing: implicit learning and memory of visual context guides spatial attention.

            Global context plays an important, but poorly understood, role in visual tasks. This study demonstrates that a robust memory for visual context exists to guide spatial attention. Global context was operationalized as the spatial layout of objects in visual search displays. Half of the configurations were repeated across blocks throughout the entire session, and targets appeared within consistent locations in these arrays. Targets appearing in learned configurations were detected more quickly. This newly discovered form of search facilitation is termed contextual cueing. Contextual cueing is driven by incidentally learned associations between spatial configurations (context) and target locations. This benefit was obtained despite chance performance for recognizing the configurations, suggesting that the memory for context was implicit. The results show how implicit learning and memory of visual context can guide spatial attention towards task-relevant aspects of a scene.
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              Active Inference: A Process Theory.

              This article describes a process theory based on active inference and belief propagation. Starting from the premise that all neuronal processing (and action selection) can be explained by maximizing Bayesian model evidence-or minimizing variational free energy-we ask whether neuronal responses can be described as a gradient descent on variational free energy. Using a standard (Markov decision process) generative model, we derive the neuronal dynamics implicit in this description and reproduce a remarkable range of well-characterized neuronal phenomena. These include repetition suppression, mismatch negativity, violation responses, place-cell activity, phase precession, theta sequences, theta-gamma coupling, evidence accumulation, race-to-bound dynamics, and transfer of dopamine responses. Furthermore, the (approximately Bayes' optimal) behavior prescribed by these dynamics has a degree of face validity, providing a formal explanation for reward seeking, context learning, and epistemic foraging. Technically, the fact that a gradient descent appears to be a valid description of neuronal activity means that variational free energy is a Lyapunov function for neuronal dynamics, which therefore conform to Hamilton's principle of least action.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                5 January 2018
                2018
                : 13
                : 1
                : e0190429
                Affiliations
                [1 ] Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London, United Kingdom
                [2 ] Institute of Cognitive Neuroscience, University College London, London, United Kingdom
                [3 ] Division of Psychiatry, University College London, London, United Kingdom
                [4 ] Scuola Internazionale Superiore di Studi Avanzati (SISSA), Trieste, Italy
                [5 ] Translational Neuromodeling Unit (TNU), Institute for Biomedical Engineering, University of Zurich and ETH Zurich, Zurich, Switzerland
                [6 ] Max Planck UCL Centre for Computational Psychiatry and Ageing Research, London, United Kingdom
                Technische Universitat Dresden, GERMANY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-9355-2052
                http://orcid.org/0000-0002-7661-8881
                http://orcid.org/0000-0003-4079-5453
                Article
                PONE-D-17-31068
                10.1371/journal.pone.0190429
                5755757
                29304087
                89815eb3-00c0-4e6c-a225-6daffa758cb5
                © 2018 Mirza et al

                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
                : 24 August 2017
                : 14 December 2017
                Page count
                Figures: 8, Tables: 0, Pages: 20
                Funding
                Funded by: Perception and Action in Complex Environments, Marie-Sklodowska-Curie Grant Agreement
                Award ID: 642961
                Award Recipient :
                MBM, RAA and KJF are members of PACE (Perception and Action in Complex Environments), an Innovative Training Network funded by the European Union’s Horizon 2020 research and innovation programme under the Marie-Sklodowska-Curie Grant Agreement No 642961. KJF is funded by the Wellcome trust (Ref: 088130/Z/09/Z). 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
                Physiology
                Sensory Physiology
                Visual System
                Eye Movements
                Medicine and Health Sciences
                Physiology
                Sensory Physiology
                Visual System
                Eye Movements
                Biology and Life Sciences
                Neuroscience
                Sensory Systems
                Visual System
                Eye Movements
                Physical Sciences
                Physics
                Thermodynamics
                Free Energy
                Biology and Life Sciences
                Behavior
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                Organisms
                Eukaryota
                Animals
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                Biology and Life Sciences
                Behavior
                Animal Behavior
                Foraging
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Foraging
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Vision
                Social Sciences
                Psychology
                Sensory Perception
                Vision
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Cats
                Medicine and Health Sciences
                Mental Health and Psychiatry
                Schizophrenia
                Custom metadata
                All the scan-path data underlying the results reported in this paper are available from the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.ph104.

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