Supplementary Eye Field Encodes Reward Prediction Error

The outcomes of many decisions are uncertain and therefore need to be evaluated. We studied this evaluation process by recording neuronal activity in the supplementary eye field (SEF) during an oculomotor gambling task. While the monkeys awaited the outcome, SEF neurons represented attributes of the chosen option, namely, its expected value and the uncertainty of this value signal. After the gamble result was revealed, a number of neurons reflected the actual reward outcome. Other neurons evaluated the outcome by encoding the difference between the reward expectation represented during the delay period and the actual reward amount (i.e., the reward prediction error). Thus, SEF encodes not only reward prediction error but also all the components necessary for its computation: the expected and the actual outcome. This suggests that SEF might actively evaluate value-based decisions in the oculomotor domain, independent of other brain regions.

• Publication year

  2012

• Venue

  Journal of Neuroscience

• Publication date

  2012-02-29

• Fields of study

  Biology, Medicine, Psychology

• Identifiers
  DOI 10.1523/JNEUROSCI.4419-11.2012PMID 22378869PMCID PMC3296227
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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• Increased activity in human visual cortex during directed attention in the absence of visual stimulation.

  1999influential reference
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  1999cited by this paper
• Amygdala circuitry in attentional and representational processes.

  1999cited by this paper
• Reinforcement learning

  1998cited by this paper
• Predictive reward signal of dopamine neurons.

  1998cited by this paper
• A Neural Substrate of Prediction and Reward

  1997cited by this paper
• A Reference Bayesian Test for Nested Hypotheses and its Relationship to the Schwarz Criterion

  1995cited by this paper
• The time course and amplitude of EPSPs evoked at synapses between pairs of CA3/CA1 neurons in the hippocampal slice

  1990cited by this paper
• Supplementary eye field as defined by intracortical microstimulation: Connections in macaques

  1990cited by this paper
• A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli.

  1980cited by this paper
• An Opponent-Process Theory of Motivation

  1978cited by this paper
• Information criteria for discriminating among alternative regression models / BEBR No. 455

  1978cited by this paper
• Applied Linear Statistical Models

  1975cited by this paper
• An opponent-process theory of motivation. I. Temporal dynamics of affect.

  1974cited by this paper
• A theory of Pavlovian conditioning : Variations in the effectiveness of reinforcement and nonreinforcement

  1972cited by this paper
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  1968cited by this paper

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• Bibliographie

  2018cites this paper
• On the Flexibility of Basic Risk Attitudes in Monkeys

  2018cites this paper
• Neuronal Correlates of Serial Decision-Making in the Supplementary Eye Field

  2018cites this paper
• Orthogonal Representations of Reward Magnitude, Certainty, and Volatility in the Macaque Orbitofrontal Cortex

  2018cites this paper
• Neuronal Risk Processing in Human and Monkey Prefrontal Cortex

  2017cites this paper
• Cortical control and performance monitoring of interrupting and redirecting movements

  2017cites this paper
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  2017cites this paper
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  2017cites this paper
• Phasic Dopamine Signaling in Action Selection and Reinforcement Learning

  2017cites this paper
• Cortical neurons multiplex reward-related signals along with sensory and motor information

  2017cites this paper
• Utility functions predict variance and skewness risk preferences in monkeys

  2016cites this paper
• Dopamine reward prediction-error signalling: a two-component response

  2016cites this paper
• Randomised prior feedback modulates neural signals of outcome monitoring

  2016influential citation
• Dopamine reward prediction error coding

  2016cites this paper
• Neural and behavioral correlates of decision confidence

  2015cites this paper
• The role of supplementary eye field in goal-directed behavior.

  2015cites this paper
• A Role For Orbitofrontal Neurons in Risky Decisions

  2015cites this paper
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  2015influential citation
• An Introduction to Neuroscientific Methods: Single-cell Recordings

  2015cites this paper
• Neuronal Reward and Decision Signals: From Theories to Data.

  2015influential citation
• Anticipating conflict: Neural correlates of a Bayesian belief and its motor consequence

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  2014cites this paper
• Performance monitoring by presupplementary and supplementary motor area during an arm movement countermanding task.

  2013influential citation
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  2013cites this paper
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  2012cites this paper
• Neuronal correlates of metacognition in primate frontal cortex.

  2012cites this paper
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