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      Value, search, persistence and model updating in anterior cingulate cortex

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          Abstract

          Dorsal anterior cingulate cortex (dACC) carries a wealth of value-related information necessary for regulating behavioral flexibility and persistence. It signals error and reward events informing decisions about switching or staying with current behavior. During decision-making, it encodes the average value of exploring alternative choices (search value), even after controlling for response selection difficulty, and during learning, it encodes the degree to which internal models of the environment and current task must be updated. dACC value signals are derived in part from the history of recent reward integrated simultaneously over multiple time scales, thereby enabling comparison of experience over the recent and extended past. Such ACC signals may instigate attentionally demanding and difficult processes such as behavioral change via interactions with prefrontal cortex. However, the signal in dACC that instigates behavioral change need not itself be a conflict or difficulty signal.

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          Most cited references53

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          The attention system of the human brain.

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            Decision making in recurrent neuronal circuits.

            Decision making has recently emerged as a central theme in neurophysiological studies of cognition, and experimental and computational work has led to the proposal of a cortical circuit mechanism of elemental decision computations. This mechanism depends on slow recurrent synaptic excitation balanced by fast feedback inhibition, which not only instantiates attractor states for forming categorical choices but also long transients for gradually accumulating evidence in favor of or against alternative options. Such a circuit endowed with reward-dependent synaptic plasticity is able to produce adaptive choice behavior. While decision threshold is a core concept for reaction time tasks, it can be dissociated from a general decision rule. Moreover, perceptual decisions and value-based economic choices are described within a unified framework in which probabilistic choices result from irregular neuronal activity as well as iterative interactions of a decision maker with an uncertain environment or other unpredictable decision makers in a social group.
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              Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning.

              The anterior cingulate and orbital cortices and the ventral striatum process different aspects of reward evaluation, whereas the dorsolateral prefrontal cortex and the dorsal striatum are involved in cognitive function. Collectively, these areas are critical to decision making. We mapped the striatal area that receives information about reward evaluation. We also explored the extent to which terminals from reward-related cortical areas converge in the striatum with those from cognitive regions. Using three-dimensional-rendered reconstructions of corticostriatal projection fields along with two-dimensional chartings, we demonstrate the reward and cognitive territories in the primate striatum and show the convergence between these cortical inputs. The results show two labeling patterns: a focal projection field that consists of densely distributed terminal patches, and a diffuse projection consisting of clusters of fibers, extending throughout a wide area of the striatum. Together, these projection fields demonstrate a remarkably large, rostral, reward-related striatal territory that reaches into the dorsal striatum. Fibers from different reward-processing and cognitive cortical areas occupy both separate and converging territories. Furthermore, the diffuse projection may serve a separate integrative function by broadly disseminating general cortical activity. These findings show that the rostral striatum is in a unique position to mediate different aspects of incentive learning. Furthermore, areas of convergence may be particularly sensitive to dopamine modulation during decision making and habit formation.
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                Author and article information

                Contributors
                (View ORCID Profile)
                Journal
                Nature Neuroscience
                Nat Neurosci
                Springer Science and Business Media LLC
                1097-6256
                1546-1726
                October 2016
                September 27 2016
                October 2016
                : 19
                : 10
                : 1280-1285
                Article
                10.1038/nn.4382
                7116891
                27669988
                9546b8a7-c23b-47b0-a3ec-7557aed7022b
                © 2016

                http://www.springer.com/tdm

                http://www.springer.com/tdm

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