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      Dopaminergic and Prefrontal Basis of Learning from Sensory Confidence and Reward Value

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          Summary

          Deciding between stimuli requires combining their learned value with one’s sensory confidence. We trained mice in a visual task that probes this combination. Mouse choices reflected not only present confidence and past rewards but also past confidence. Their behavior conformed to a model that combines signal detection with reinforcement learning. In the model, the predicted value of the chosen option is the product of sensory confidence and learned value. We found precise correlates of this variable in the pre-outcome activity of midbrain dopamine neurons and of medial prefrontal cortical neurons. However, only the latter played a causal role: inactivating medial prefrontal cortex before outcome strengthened learning from the outcome. Dopamine neurons played a causal role only after outcome, when they encoded reward prediction errors graded by confidence, influencing subsequent choices. These results reveal neural signals that combine reward value with sensory confidence and guide subsequent learning.

          Highlights

          • Mouse choices depend on present confidence, learned rewards, and past confidence

          • Choices constrain a model that predicts activity in prefrontal and dopamine neurons

          • Learning relies on prefrontal signals encoding predicted value

          • Learning relies on dopamine signals encoding prediction error but not predicted value

          Abstract

          Lak et al. model the choices made by mice in a visual task with biased rewards and establish neural correlates of the model’s variables, revealing how choices and learning depend on sensory confidence and reward value.

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          Most cited references40

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          Neurons in the orbitofrontal cortex encode economic value.

          Economic choice is the behaviour observed when individuals select one among many available options. There is no intrinsically 'correct' answer: economic choice depends on subjective preferences. This behaviour is traditionally the object of economic analysis and is also of primary interest in psychology. However, the underlying mental processes and neuronal mechanisms are not well understood. Theories of human and animal choice have a cornerstone in the concept of 'value'. Consider, for example, a monkey offered one raisin versus one piece of apple: behavioural evidence suggests that the animal chooses by assigning values to the two options. But where and how values are represented in the brain is unclear. Here we show that, during economic choice, neurons in the orbitofrontal cortex (OFC) encode the value of offered and chosen goods. Notably, OFC neurons encode value independently of visuospatial factors and motor responses. If a monkey chooses between A and B, neurons in the OFC encode the value of the two goods independently of whether A is presented on the right and B on the left, or vice versa. This trait distinguishes the OFC from other brain areas in which value modulates activity related to sensory or motor processes. Our results have broad implications for possible psychological models, suggesting that economic choice is essentially choice between goods rather than choice between actions. In this framework, neurons in the OFC seem to be a good candidate network for value assignment underlying economic choice.
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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 Causal Link Between Prediction Errors, Dopamine Neurons and Learning

              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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                Author and article information

                Contributors
                Journal
                Neuron
                Neuron
                Neuron
                Cell Press
                0896-6273
                1097-4199
                19 February 2020
                19 February 2020
                : 105
                : 4
                : 700-711.e6
                Affiliations
                [1 ]UCL Institute of Ophthalmology, University College London, London WC1E 6BT, UK
                [2 ]UCL Queen Square Institute of Neurology, University College London, London WC1E 6BT, UK
                [3 ]Centre for Systems Neuroscience, University of Leicester, Leicester LE1 7RH, UK
                [4 ]Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USA
                Author notes
                []Corresponding author armin.lak@ 123456dpag.ox.ac.uk
                [5]

                Present address: Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK

                [6]

                Senior author

                [7]

                Lead Contact

                Article
                S0896-6273(19)30982-1
                10.1016/j.neuron.2019.11.018
                7031700
                31859030
                09ab3bc4-de5e-4828-9350-b21be961d5b3
                © 2019 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 11 April 2019
                : 4 September 2019
                : 11 November 2019
                Categories
                Article

                Neurosciences
                reinforcement learning,decision confidence,psychophysics,mice,electrophysiology,calcium imaging,optogenetics

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