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      A Causal Link Between Prediction Errors, Dopamine Neurons and Learning

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          Abstract

          Situations where rewards are unexpectedly obtained or withheld represent opportunities for new learning. Often, this learning includes identifying cues that predict reward availability. Unexpected rewards strongly activate midbrain dopamine neurons. This phasic signal is proposed to support learning about antecedent cues by signaling discrepancies between actual and expected outcomes, termed a reward prediction error. However, it is unknown whether dopamine neuron prediction error signaling and cue-reward learning are causally linked. To test this hypothesis, we manipulated dopamine neuron activity in rats in two behavioral procedures, associative blocking and extinction, that illustrate the essential function of prediction errors in learning. We observed that optogenetic activation of dopamine neurons concurrent with reward delivery, mimicking a prediction error, was sufficient to cause long-lasting increases in cue-elicited reward-seeking behavior. Our findings establish a causal role for temporally-precise dopamine neuron signaling in cue-reward learning, bridging a critical gap between experimental evidence and influential theoretical frameworks.

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          Most cited references38

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          Modulation of striatal projection systems by dopamine.

          The basal ganglia are a chain of subcortical nuclei that facilitate action selection. Two striatal projection systems--so-called direct and indirect pathways--form the functional backbone of the basal ganglia circuit. Twenty years ago, investigators proposed that the striatum's ability to use dopamine (DA) rise and fall to control action selection was due to the segregation of D(1) and D(2) DA receptors in direct- and indirect-pathway spiny projection neurons. Although this hypothesis sparked a debate, the evidence that has accumulated since then clearly supports this model. Recent advances in the means of marking neural circuits with optical or molecular reporters have revealed a clear-cut dichotomy between these two cell types at the molecular, anatomical, and physiological levels. The contrast provided by these studies has provided new insights into how the striatum responds to fluctuations in DA signaling and how diseases that alter this signaling change striatal function.
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            Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning.

            Natural rewards and drugs of abuse can alter dopamine signaling, and ventral tegmental area (VTA) dopaminergic neurons are known to fire action potentials tonically or phasically under different behavioral conditions. However, without technology to control specific neurons with appropriate temporal precision in freely behaving mammals, the causal role of these action potential patterns in driving behavioral changes has been unclear. We used optogenetic tools to selectively stimulate VTA dopaminergic neuron action potential firing in freely behaving mammals. We found that phasic activation of these neurons was sufficient to drive behavioral conditioning and elicited dopamine transients with magnitudes not achieved by longer, lower-frequency spiking. These results demonstrate that phasic dopaminergic activity is sufficient to mediate mammalian behavioral conditioning.
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              A framework for mesencephalic dopamine systems based on predictive Hebbian learning.

              We develop a theoretical framework that shows how mesencephalic dopamine systems could distribute to their targets a signal that represents information about future expectations. In particular, we show how activity in the cerebral cortex can make predictions about future receipt of reward and how fluctuations in the activity levels of neurons in diffuse dopamine systems above and below baseline levels would represent errors in these predictions that are delivered to cortical and subcortical targets. We present a model for how such errors could be constructed in a real brain that is consistent with physiological results for a subset of dopaminergic neurons located in the ventral tegmental area and surrounding dopaminergic neurons. The theory also makes testable predictions about human choice behavior on a simple decision-making task. Furthermore, we show that, through a simple influence on synaptic plasticity, fluctuations in dopamine release can act to change the predictions in an appropriate manner.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                3 June 2013
                26 May 2013
                July 2013
                26 November 2013
                : 16
                : 7
                : 10.1038/nn.3413
                Affiliations
                [1 ]Ernest Gallo Clinic & Research Center, University of California, San Francisco, San Francisco, CA 94143, USA
                [2 ]Graduate program in Neuroscience, University of California, San Francisco, San Francisco CA 94143, USA.
                [3 ]Dept. of Neurology, University of California, San Francisco, San Francisco CA 94143, USA.
                [4 ]Wheeler Center for the Neurobiology of Addiction, University of California, San Francisco, San Francisco CA 94143, USA.
                [5 ]Princeton Neuroscience Institute & Department of Psychology, Princeton University, Princeton, NJ, 08544, USA.
                [6 ]Department of Bioengineering, Department of Psychiatry and Behavioral Sciences, Howard Hughes Medical Institute, CNC Program, Stanford University, Stanford, CA 94305, USA.
                Author notes
                [] Correspondence to: pjanak@ 123456gallo.ucsf.edu
                [*]

                Denotes equal contribution.

                Article
                NIHMS475445
                10.1038/nn.3413
                3705924
                23708143
                00895e62-db0c-4592-896f-5e01e664361e

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