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      Reward-based training of recurrent neural networks for cognitive and value-based tasks

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          Abstract

          Trained neural network models, which exhibit features of neural activity recorded from behaving animals, may provide insights into the circuit mechanisms of cognitive functions through systematic analysis of network activity and connectivity. However, in contrast to the graded error signals commonly used to train networks through supervised learning, animals learn from reward feedback on definite actions through reinforcement learning. Reward maximization is particularly relevant when optimal behavior depends on an animal’s internal judgment of confidence or subjective preferences. Here, we implement reward-based training of recurrent neural networks in which a value network guides learning by using the activity of the decision network to predict future reward. We show that such models capture behavioral and electrophysiological findings from well-known experimental paradigms. Our work provides a unified framework for investigating diverse cognitive and value-based computations, and predicts a role for value representation that is essential for learning, but not executing, a task.

          DOI: http://dx.doi.org/10.7554/eLife.21492.001

          eLife digest

          A major goal in neuroscience is to understand the relationship between an animal’s behavior and how this is encoded in the brain. Therefore, a typical experiment involves training an animal to perform a task and recording the activity of its neurons – brain cells – while the animal carries out the task. To complement these experimental results, researchers “train” artificial neural networks – simplified mathematical models of the brain that consist of simple neuron-like units – to simulate the same tasks on a computer. Unlike real brains, artificial neural networks provide complete access to the “neural circuits” responsible for a behavior, offering a way to study and manipulate the behavior in the circuit.

          One open issue about this approach has been the way in which the artificial networks are trained. In a process known as reinforcement learning, animals learn from rewards (such as juice) that they receive when they choose actions that lead to the successful completion of a task. By contrast, the artificial networks are explicitly told the correct action. In addition to differing from how animals learn, this limits the types of behavior that can be studied using artificial neural networks.

          Recent advances in the field of machine learning that combine reinforcement learning with artificial neural networks have now allowed Song et al. to train artificial networks to perform tasks in a way that mimics the way that animals learn. The networks consisted of two parts: a “decision network” that uses sensory information to select actions that lead to the greatest reward, and a “value network” that predicts how rewarding an action will be. Song et al. found that the resulting artificial “brain activity” closely resembled the activity found in the brains of animals, confirming that this method of training artificial neural networks may be a useful tool for neuroscientists who study the relationship between brains and behavior.

          The training method explored by Song et al. represents only one step forward in developing artificial neural networks that resemble the real brain. In particular, neural networks modify connections between units in a vastly different way to the methods used by biological brains to alter the connections between neurons. Future work will be needed to bridge this gap.

          DOI: http://dx.doi.org/10.7554/eLife.21492.002

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          Learning Phrase Representations using RNN Encoder–Decoder for Statistical Machine Translation

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            The importance of mixed selectivity in complex cognitive tasks.

            Single-neuron activity in the prefrontal cortex (PFC) is tuned to mixtures of multiple task-related aspects. Such mixed selectivity is highly heterogeneous, seemingly disordered and therefore difficult to interpret. We analysed the neural activity recorded in monkeys during an object sequence memory task to identify a role of mixed selectivity in subserving the cognitive functions ascribed to the PFC. We show that mixed selectivity neurons encode distributed information about all task-relevant aspects. Each aspect can be decoded from the population of neurons even when single-cell selectivity to that aspect is eliminated. Moreover, mixed selectivity offers a significant computational advantage over specialized responses in terms of the repertoire of input-output functions implementable by readout neurons. This advantage originates from the highly diverse nonlinear selectivity to mixtures of task-relevant variables, a signature of high-dimensional neural representations. Crucially, this dimensionality is predictive of animal behaviour as it collapses in error trials. Our findings recommend a shift of focus for future studies from neurons that have easily interpretable response tuning to the widely observed, but rarely analysed, mixed selectivity neurons.
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              Planning and acting in partially observable stochastic domains

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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                13 January 2017
                2017
                : 6
                : e21492
                Affiliations
                [1 ]deptCenter for Neural Science , New York University , New York, United States
                [2 ]deptNYU-ECNU Institute of Brain and Cognitive Science , NYU Shanghai , Shanghai, China
                [3]University College London , United Kingdom
                [4]University College London , United Kingdom
                Author notes
                Author information
                http://orcid.org/0000-0003-3124-8474
                Article
                21492
                10.7554/eLife.21492
                5293493
                28084991
                11990118-6add-4413-8917-6792d62a9240
                © 2017, Song et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 13 September 2016
                : 12 January 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000006, Office of Naval Research;
                Award ID: N00014-13-1-0297
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100006785, Google;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                2.5
                A two-part neural network models reward-based training and provides a unified framework in which to study diverse computations that can be compared to electrophysiological recordings from behaving animals.

                Life sciences
                recurrent neural network,reinforcement learning,prefrontal cortex,decision making,orbitofrontal cortex,working memory,other

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