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      Learning Predictive Statistics: Strategies and Brain Mechanisms

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          Abstract

          When immersed in a new environment, we are challenged to decipher initially incomprehensible streams of sensory information. However, quite rapidly, the brain finds structure and meaning in these incoming signals, helping us to predict and prepare ourselves for future actions. This skill relies on extracting the statistics of event streams in the environment that contain regularities of variable complexity from simple repetitive patterns to complex probabilistic combinations. Here, we test the brain mechanisms that mediate our ability to adapt to the environment's statistics and predict upcoming events. By combining behavioral training and multisession fMRI in human participants (male and female), we track the corticostriatal mechanisms that mediate learning of temporal sequences as they change in structure complexity. We show that learning of predictive structures relates to individual decision strategy; that is, selecting the most probable outcome in a given context (maximizing) versus matching the exact sequence statistics. These strategies engage distinct human brain regions: maximizing engages dorsolateral prefrontal, cingulate, sensory–motor regions, and basal ganglia (dorsal caudate, putamen), whereas matching engages occipitotemporal regions (including the hippocampus) and basal ganglia (ventral caudate). Our findings provide evidence for distinct corticostriatal mechanisms that facilitate our ability to extract behaviorally relevant statistics to make predictions.

          SIGNIFICANCE STATEMENT Making predictions about future events relies on interpreting streams of information that may initially appear incomprehensible. Past work has studied how humans identify repetitive patterns and associative pairings. However, the natural environment contains regularities that vary in complexity from simple repetition to complex probabilistic combinations. Here, we combine behavior and multisession fMRI to track the brain mechanisms that mediate our ability to adapt to changes in the environment's statistics. We provide evidence for an alternate route for learning complex temporal statistics: extracting the most probable outcome in a given context is implemented by interactions between executive and motor corticostriatal mechanisms compared with visual corticostriatal circuits (including hippocampal cortex) that support learning of the exact temporal statistics.

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          Parallel organization of functionally segregated circuits linking basal ganglia and cortex.

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            Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action.

            Recent behavioral studies in both humans and rodents have found evidence that performance in decision-making tasks depends on two different learning processes; one encoding the relationship between actions and their consequences and a second involving the formation of stimulus-response associations. These learning processes are thought to govern goal-directed and habitual actions, respectively, and have been found to depend on homologous corticostriatal networks in these species. Thus, recent research using comparable behavioral tasks in both humans and rats has implicated homologous regions of cortex (medial prefrontal cortex/medial orbital cortex in humans and prelimbic cortex in rats) and of dorsal striatum (anterior caudate in humans and dorsomedial striatum in rats) in goal-directed action and in the control of habitual actions (posterior lateral putamen in humans and dorsolateral striatum in rats). These learning processes have been argued to be antagonistic or competing because their control over performance appears to be all or none. Nevertheless, evidence has started to accumulate suggesting that they may at times compete and at others cooperate in the selection and subsequent evaluation of actions necessary for normal choice performance. It appears likely that cooperation or competition between these sources of action control depends not only on local interactions in dorsal striatum but also on the cortico-basal ganglia network within which the striatum is embedded and that mediates the integration of learning with basic motivational and emotional processes. The neural basis of the integration of learning and motivation in choice and decision-making is still controversial and we review some recent hypotheses relating to this issue.
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              Attentional requirements of learning: Evidence from performance measures

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                Author and article information

                Journal
                J Neurosci
                J. Neurosci
                jneuro
                jneurosci
                J. Neurosci
                The Journal of Neuroscience
                Society for Neuroscience
                0270-6474
                1529-2401
                30 August 2017
                30 August 2017
                : 37
                : 35
                : 8412-8427
                Affiliations
                [1] 1Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China,
                [2] 2Department of Psychology, University of Cambridge, Cambridge CB2 3EB, United Kingdom,
                [3] 3Department of Mathematical Sciences, Xi'an Jiaotong-Liverpool University, Suzhou 215123, China, and
                [4] 4School of Computer Science, University of Birmingham, Birmingham B15 2TT, United Kingdom
                Author notes
                Correspondence should be addressed to Zoe Kourtzi, Department of Psychology, University of Cambridge, Downing Site, Cambridge CB2 3EB, UK. zk240@ 123456cam.ac.uk

                Author contributions: R.W., Y.S., P.T., A.E.W., and Z.K. designed research; R.W. and Y.S. performed research; R.W. and Y.S. analyzed data; R.W., Y.S., P.T., A.E.W., and Z.K. wrote the paper.

                Author information
                http://orcid.org/0000-0002-9299-0034
                http://orcid.org/0000-0002-7559-3299
                http://orcid.org/0000-0001-9441-7832
                Article
                0144-17
                10.1523/JNEUROSCI.0144-17.2017
                5577855
                28760866
                ec270f74-7fd2-4c07-a6b5-f82b8515c4d4
                Copyright © 2017 Wang et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 17 January 2017
                : 18 May 2017
                : 26 May 2017
                Categories
                Research Articles
                Behavioral/Cognitive

                fmri,learning,prediction,vision
                fmri, learning, prediction, vision

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