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      Catecholaminergic Regulation of Learning Rate in a Dynamic Environment

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          Abstract

          Adaptive behavior in a changing world requires flexibly adapting one’s rate of learning to the rate of environmental change. Recent studies have examined the computational mechanisms by which various environmental factors determine the impact of new outcomes on existing beliefs (i.e., the ‘learning rate’). However, the brain mechanisms, and in particular the neuromodulators, involved in this process are still largely unknown. The brain-wide neurophysiological effects of the catecholamines norepinephrine and dopamine on stimulus-evoked cortical responses suggest that the catecholamine systems are well positioned to regulate learning about environmental change, but more direct evidence for a role of this system is scant. Here, we report evidence from a study employing pharmacology, scalp electrophysiology and computational modeling (N = 32) that suggests an important role for catecholamines in learning rate regulation. We found that the P3 component of the EEG—an electrophysiological index of outcome-evoked phasic catecholamine release in the cortex—predicted learning rate, and formally mediated the effect of prediction-error magnitude on learning rate. P3 amplitude also mediated the effects of two computational variables—capturing the unexpectedness of an outcome and the uncertainty of a preexisting belief—on learning rate. Furthermore, a pharmacological manipulation of catecholamine activity affected learning rate following unanticipated task changes, in a way that depended on participants’ baseline learning rate. Our findings provide converging evidence for a causal role of the human catecholamine systems in learning-rate regulation as a function of environmental change.

          Author Summary

          Belief updating in response to changes in the environment is crucial for adaptive behavior. We examined the role of the human catecholamine (norepinephrine and dopamine) systems in this process, using a combination of pharmacology, scalp electrophysiology and computational modeling. We found that the P3 component of the event-related potential—an electrophysiological index of phasic catecholamine release in the cortex—predicted learning rate and mediated the effect of prediction-error magnitude on learning rate. Furthermore, a pharmacological manipulation of catecholamine activity affected learning rate following unanticipated task changes, in a way that depended on participants’ natural learning rate. These findings may reflect the catecholaminergic regulation of belief updating following environmental change.

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          Most cited references59

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          Inverted-U-shaped dopamine actions on human working memory and cognitive control.

          Brain dopamine (DA) has long been implicated in cognitive control processes, including working memory. However, the precise role of DA in cognition is not well-understood, partly because there is large variability in the response to dopaminergic drugs both across different behaviors and across different individuals. We review evidence from a series of studies with experimental animals, healthy humans, and patients with Parkinson's disease, which highlight two important factors that contribute to this large variability. First, the existence of an optimum DA level for cognitive function implicates the need to take into account baseline levels of DA when isolating the effects of DA. Second, cognitive control is a multifactorial phenomenon, requiring a dynamic balance between cognitive stability and cognitive flexibility. These distinct components might implicate the prefrontal cortex and the striatum, respectively. Manipulating DA will thus have paradoxical consequences for distinct cognitive control processes, depending on distinct basal or optimal levels of DA in different brain regions. Copyright © 2011 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
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            Decision making, the P3, and the locus coeruleus-norepinephrine system.

            Psychologists and neuroscientists have had a long-standing interest in the P3, a prominent component of the event-related brain potential. This review aims to integrate knowledge regarding the neural basis of the P3 and to elucidate its functional role in information processing. The authors review evidence suggesting that the P3 reflects phasic activity of the neuromodulatory locus coeruleus-norepinephrine (LC-NE) system. They discuss the P3 literature in the light of empirical findings and a recent theory regarding the information-processing function of the LC-NE phasic response. The theoretical framework emerging from this research synthesis suggests that the P3 reflects the response of the LC-NE system to the outcome of internal decision-making processes and the consequent effects of noradrenergic potentiation of information processing. Copyright 2005 APA, all rights reserved.
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              The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes.

              Through a widespread efferent projection system, the locus coeruleus-noradrenergic system supplies norepinephrine throughout the central nervous system. Initial studies provided critical insight into the basic organization and properties of this system. More recent work identifies a complicated array of behavioral and electrophysiological actions that have in common the facilitation of processing of relevant, or salient, information. This involves two basic levels of action. First, the system contributes to the initiation and maintenance of behavioral and forebrain neuronal activity states appropriate for the collection of sensory information (e.g. waking). Second, within the waking state, this system modulates the collection and processing of salient sensory information through a diversity of concentration-dependent actions within cortical and subcortical sensory, attention, and memory circuits. Norepinephrine-dependent modulation of long-term alterations in synaptic strength, gene transcription and other processes suggest a potentially critical role of this neurotransmitter system in experience-dependent alterations in neural function and behavior. The ability of a given stimulus to increase locus coeruleus discharge activity appears independent of affective valence (appetitive vs. aversive). Combined, these observations suggest that the locus coeruleus-noradrenergic system is a critical component of the neural architecture supporting interaction with, and navigation through, a complex world. These observations further suggest that dysregulation of locus coeruleus-noradrenergic neurotransmission may contribute to cognitive and/or arousal dysfunction associated with a variety of psychiatric disorders, including attention-deficit hyperactivity disorder, sleep and arousal disorders, as well as certain affective disorders, including post-traumatic stress disorder. Independent of an etiological role in these disorders, the locus coeruleus-noradrenergic system represents an appropriate target for pharmacological treatment of specific attention, memory and/or arousal dysfunction associated with a variety of behavioral/cognitive disorders.
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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, CA USA )
                1553-734X
                1553-7358
                28 October 2016
                October 2016
                : 12
                : 10
                : e1005171
                Affiliations
                [1 ]Cognitive Psychology Unit, Institute of Psychology, Leiden University; and Leiden Institute for Brain and Cognition, Leiden University, Leiden, the Netherlands
                [2 ]Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
                [3 ]Department of Cognitive, Linguistic & Psychological Sciences, Brown University, Providence, RI, United States of America
                [4 ]Department of Psychology, University of California, Berkeley, United States of America
                [5 ]Department of Education Sciences, Vrije Universiteit Amsterdam, The Netherlands
                Oxford University, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                • Conceptualization: MJ SN.

                • Formal analysis: MJ PRM MRN.

                • Funding acquisition: SN MJ.

                • Investigation: MRG.

                • Methodology: MJ MRN.

                • Project administration: MJ SN.

                • Resources: MM.

                • Supervision: SN MJ.

                • Validation: MJ.

                • Visualization: MJ PRM.

                • Writing – original draft: MJ.

                • Writing – review & editing: PRM MRN MRG MM SN.

                Author information
                http://orcid.org/0000-0003-1963-185X
                Article
                PCOMPBIOL-D-16-00512
                10.1371/journal.pcbi.1005171
                5085041
                27792728
                63569c93-262e-411b-b33e-98f6a3571f84
                © 2016 Jepma 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
                : 29 March 2016
                : 27 September 2016
                Page count
                Figures: 5, Tables: 0, Pages: 24
                Funding
                This research was supported by a Consolidator Grant of the European Research Council (SN) and by a VENI (MJ) grant of the Netherlands Organization for Scientific Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                The single-trial behavioral and P3 amplitude data can be found at the Dryad repository, doi: 10.5061/dryad.0r9p1

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