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      Reasoning, Learning, and Creativity: Frontal Lobe Function and Human Decision-Making

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      PLoS Biology
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          Abstract

          Computational modeling and behavioral experimentation suggest that human frontal lobe function is capable of monitoring three or four concurrent behavioral strategies in order to select the most suitable one during decision-making.

          Abstract

          The frontal lobes subserve decision-making and executive control—that is, the selection and coordination of goal-directed behaviors. Current models of frontal executive function, however, do not explain human decision-making in everyday environments featuring uncertain, changing, and especially open-ended situations. Here, we propose a computational model of human executive function that clarifies this issue. Using behavioral experiments, we show that unlike others, the proposed model predicts human decisions and their variations across individuals in naturalistic situations. The model reveals that for driving action, the human frontal function monitors up to three/four concurrent behavioral strategies and infers online their ability to predict action outcomes: whenever one appears more reliable than unreliable, this strategy is chosen to guide the selection and learning of actions that maximize rewards. Otherwise, a new behavioral strategy is tentatively formed, partly from those stored in long-term memory, then probed, and if competitive confirmed to subsequently drive action. Thus, the human executive function has a monitoring capacity limited to three or four behavioral strategies. This limitation is compensated by the binary structure of executive control that in ambiguous and unknown situations promotes the exploration and creation of new behavioral strategies. The results support a model of human frontal function that integrates reasoning, learning, and creative abilities in the service of decision-making and adaptive behavior.

          Author Summary

          Reasoning, learning, and creativity are hallmarks of human intelligence. These abilities involve the frontal lobe of the brain, but it remains unclear how the frontal lobes function in uncertain or open-ended situations. We propose here a computational model of human executive function that integrates multiple processes during decision-making, such as expectedness of uncertainty, task switching, and reinforcement learning. The model was tested in behavioral experiments and accounts for human decisions and their variations across individuals. The model reveals that executive function is capable of monitoring three or four concurrent behavioral strategies and infers online strategies' ability to predict action outcomes. If one strategy appears to reliably predict action outcomes, then it is chosen and possibly adjusted; otherwise a new strategy is tentatively formed, probed, and chosen instead. Thus, human frontal function has a monitoring capacity limited to three or four behavioral strategies. The results support a model of frontal executive function that explains the role and limitations of human reasoning, learning, and creative abilities in decision-making and adaptive behavior.

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          Most cited references48

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          An information theoretical approach to prefrontal executive function.

          The prefrontal cortex subserves executive control--that is, the ability to select actions or thoughts in relation to internal goals. Here, we propose a theory that draws upon concepts from information theory to describe the architecture of executive control in the lateral prefrontal cortex. Supported by evidence from brain imaging in human subjects, the model proposes that action selection is guided by hierarchically ordered control signals, processed in a network of brain regions organized along the anterior-posterior axis of the lateral prefrontal cortex. The theory clarifies how executive control can operate as a unitary function, despite the requirement that information be integrated across multiple distinct, functionally specialized prefrontal regions.
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            Choice, uncertainty and value in prefrontal and cingulate cortex.

            Reinforcement learning models that focus on the striatum and dopamine can predict the choices of animals and people. Representations of reward expectation and of reward prediction errors that are pertinent to decision making, however, are not confined to these regions but are also found in prefrontal and cingulate cortex. Moreover, decisions are not guided solely by the magnitude of the reward that is expected. Uncertainty in the estimate of the reward expectation, the value of information that might be gained by taking a course of action and the cost of an action all influence the manner in which decisions are made through prefrontal and cingulate cortex.
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              Frontal lobes and human memory: insights from functional neuroimaging.

              The new functional neuroimaging techniques, PET and functional MRI (fMRI), offer sufficient experimental flexibility and spatial resolution to explore the functional neuroanatomical bases of different memory stages and processes. They have had a particular impact on our understanding of the role of the frontal cortex in memory processing. We review the insights that have been gained, and attempt a synthesis of the findings from functional imaging studies of working memory, encoding in episodic memory and retrieval from episodic memory. Though these different aspects of memory have usually been studied in isolation, we suggest that there is sufficient convergence with respect to frontal activations to make such a synthesis worthwhile. We concentrate in particular on three regions of the lateral frontal cortex--ventrolateral, dorsolateral and anterior--that are consistently activated in these studies, and attribute these activations to the updating/maintenance of information, the selection/manipulation/monitoring of that information, and the selection of processes/subgoals, respectively. We also acknowledge a number of empirical inconsistencies associated with this synthesis, and suggest possible reasons for these. More generally, we predict that the resolution of questions concerning the functional neuroanatomical subdivisions of the frontal cortex will ultimately depend on a fuller cognitive psychological fractionation of memory control processes, an enterprise that will be guided and tested by experimentation. We expect that the neuroimaging techniques will provide an important part of this enterprise.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                March 2012
                March 2012
                27 March 2012
                : 10
                : 3
                : e1001293
                Affiliations
                [1 ]Département d'Etudes Cognitives, Ecole Normale Superieure, Paris, France
                [2 ]Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island, United States of America
                [3 ]Université Pierre et Marie Curie, Paris, France
                [4 ]Laboratoire de Neurosciences Cognitives, Institut National de la Santé et de la Recherche Médicale, Paris, France
                California Institute of Technology, United States of America
                Author notes

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: AC EK. Performed the experiments: AC. Analyzed the data: AC EK. Contributed reagents/materials/analysis tools: AC EK. Wrote the paper: AC EK. Computational modeling: AC EK.

                Article
                PBIOLOGY-D-11-03007
                10.1371/journal.pbio.1001293
                3313946
                22479152
                5b265703-f384-451b-a52d-599186c372c5
                Collins, Koechlin. 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 July 2011
                : 15 February 2012
                Page count
                Pages: 16
                Categories
                Research Article
                Biology
                Computational Biology
                Neuroscience
                Cognitive Neuroscience
                Social and Behavioral Sciences
                Psychology

                Life sciences
                Life sciences

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