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      Anticipation of novelty recruits reward system and hippocampus while promoting recollection

      a , b ,   a , b , c , *

      Neuroimage

      Academic Press

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          Abstract

          The dopaminergic midbrain, which comprises the substantia nigra and ventral tegmental area (SN/VTA), plays a central role in reward processing. This region is also activated by novel stimuli, raising the possibility that novelty and reward have shared functional properties. It is currently unclear whether functional aspects of reward processing in the SN/VTA, namely, activation by unexpected rewards and cues that predict reward, also characterize novelty processing. To address this question, we conducted an fMRI experiment during which subjects viewed symbolic cues that predicted either novel or familiar images of scenes with 75% validity. We show that SN/VTA was activated by cues predicting novel images as well as by unexpected novel images that followed familiarity-predictive cues, an ‘unexpected novelty’ response. The hippocampus, a region implicated in detecting and encoding novel stimuli, showed an anticipatory novelty response but differed from the response profile of SN/VTA in responding at outcome to expected and ‘unexpected’ novelty. In a behavioral extension of the experiment, recollection increased relative to familiarity when comparing delayed recognition memory for anticipated novel stimuli with unexpected novel stimuli. These data reveal commonalities in SN/VTA responses to anticipating reward and anticipating novel stimuli. We suggest that this anticipatory response codes a motivational exploratory novelty signal that, together with anticipatory activation of the hippocampus, leads to enhanced encoding of novel events. In more general terms, the data suggest that dopaminergic processing of novelty might be important in driving exploration of new environments.

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          Most cited references 41

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          Memory and consciousness.

           Endel Tulving (1985)
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            Getting formal with dopamine and reward.

            Recent neurophysiological studies reveal that neurons in certain brain structures carry specific signals about past and future rewards. Dopamine neurons display a short-latency, phasic reward signal indicating the difference between actual and predicted rewards. The signal is useful for enhancing neuronal processing and learning behavioral reactions. It is distinctly different from dopamine's tonic enabling of numerous behavioral processes. Neurons in the striatum, frontal cortex, and amygdala also process reward information but provide more differentiated information for identifying and anticipating rewards and organizing goal-directed behavior. The different reward signals have complementary functions, and the optimal use of rewards in voluntary behavior would benefit from interactions between the signals. Addictive psychostimulant drugs may exert their action by amplifying the dopamine reward signal.
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              Dissociation of reward anticipation and outcome with event-related fMRI.

              Reward processing involves both appetitive and consummatory phases. We sought to examine whether reward anticipation vs outcomes would recruit different regions of ventral forebrain circuitry using event-related fMRI. Nine healthy volunteers participated in a monetary incentive delays task in which they either responded to a cued target for monetary reward, responded to a cued target for no reward, or did not respond to a cued target during scanning. Multiple regression analyses indicated that while anticipation of reward vs non-reward activated foci in the ventral striatum, reward vs non-reward outcomes activated foci in the ventromedial frontal cortex. These findings suggest that reward anticipation and outcomes may differentially recruit distinct regions that lie along the trajectory of ascending dopamine projections.
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                Author and article information

                Contributors
                Journal
                Neuroimage
                Neuroimage
                Academic Press
                1053-8119
                1095-9572
                15 October 2007
                15 October 2007
                : 38
                : 1-9
                : 194-202
                Affiliations
                [a ]Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK
                [b ]Institute of Cognitive Neuroscience and Department of Psychology, University College London, 17 Queen Square, London WC1N 3AR, UK
                [c ]Department of Neurology II and Centre for Advanced Imaging, Otto von Guericke University, Leipziger Str. 44, 39120 Magdeburg, Germany
                Author notes
                [* ]Corresponding author. Institute of Cognitive Neuroscience, University College London, 17 Queen Square, London WC1N 3AR, UK. Fax: +44 20 7679 1160. e.duzel@ 123456ucl.ac.uk
                Article
                YNIMG4765
                10.1016/j.neuroimage.2007.06.038
                2706325
                17764976
                © 2007 Elsevier Inc.

                This document may be redistributed and reused, subject to certain conditions.

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                Neurosciences

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