Neural correlates, computation and behavioural impact of decision confidence

Humans and other animals must often make decisions on the basis of imperfect evidence. Statisticians use measures such as P values to assign degrees of confidence to propositions, but little is known about how the brain computes confidence estimates about decisions. We explored this issue using behavioural analysis and neural recordings in rats in combination with computational modelling. Subjects were trained to perform an odour categorization task that allowed decision confidence to be manipulated by varying the distance of the test stimulus to the category boundary. To understand how confidence could be computed along with the choice itself, using standard models of decision-making, we defined a simple measure that quantified the quality of the evidence contributing to a particular decision. Here we show that the firing rates of many single neurons in the orbitofrontal cortex match closely to the predictions of confidence models and cannot be readily explained by alternative mechanisms, such as learning stimulus–outcome associations. Moreover, when tested using a delayed reward version of the task, we found that rats’ willingness to wait for rewards increased with confidence, as predicted by the theoretical model. These results indicate that confidence estimates, previously suggested to require ‘metacognition’ and conscious awareness, are available even in the rodent brain, can be computed with relatively simple operations, and can drive adaptive behaviour. We suggest that confidence estimation may be a fundamental and ubiquitous component of decision-making.

[1]  D. Vickers,et al.  Evidence for an accumulator model of psychophysical discrimination. , 1970, Ergonomics.

[2]  A. Tversky,et al.  Judgment under Uncertainty: Heuristics and Biases , 1974, Science.

[3]  P. Hansen Rank-Deficient and Discrete Ill-Posed Problems: Numerical Aspects of Linear Inversion , 1987 .

[4]  S J Luck,et al.  Mechanisms of visual-spatial attention: resource allocation or uncertainty reduction? , 1996, Journal of experimental psychology. Human perception and performance.

[5]  Per Christian Hansen,et al.  Rank-Deficient and Discrete Ill-Posed Problems , 1996 .

[6]  A. Damasio,et al.  Deciding Advantageously Before Knowing the Advantageous Strategy , 1997, Science.

[7]  Gideon Keren,et al.  On The Calibration of Probability Judgments: Some Critical Comments and Alternative Perspectives , 1997 .

[8]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.

[9]  Alexandre Pouget,et al.  Probabilistic Interpretation of Population Codes , 1996, Neural Computation.

[10]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

[11]  W. Schultz,et al.  Relative reward preference in primate orbitofrontal cortex , 1999, Nature.

[12]  Debashis Kushary,et al.  Bootstrap Methods and Their Application , 2000, Technometrics.

[13]  M. Laubach,et al.  Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task , 2000, Nature.

[14]  S. Kakade,et al.  Learning and selective attention , 2000, Nature Neuroscience.

[15]  K. Hikosaka,et al.  Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. , 2000, Cerebral cortex.

[16]  R. Hampton Rhesus monkeys know when they remember , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  H. Critchley,et al.  Neural Activity in the Human Brain Relating to Uncertainty and Arousal during Anticipation , 2001, Neuron.

[18]  P. Glimcher Decisions, Uncertainty, and the Brain: The Science of Neuroeconomics , 2003 .

[19]  J. D. Smith,et al.  The comparative psychology of uncertainty monitoring and metacognition. , 2003, The Behavioral and brain sciences.

[20]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[21]  E. Miller,et al.  Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task , 2003, The European journal of neuroscience.

[22]  Z. Mainen,et al.  Speed and accuracy of olfactory discrimination in the rat , 2003, Nature Neuroscience.

[23]  W. Schultz,et al.  Discrete Coding of Reward Probability and Uncertainty by Dopamine Neurons , 2003, Science.

[24]  M. Shadlen,et al.  A role for neural integrators in perceptual decision making. , 2003, Cerebral cortex.

[25]  W. Newsome,et al.  Matching Behavior and the Representation of Value in the Parietal Cortex , 2004, Science.

[26]  D. Knill,et al.  The Bayesian brain: the role of uncertainty in neural coding and computation , 2004, Trends in Neurosciences.

[27]  D. Barraclough,et al.  Prefrontal cortex and decision making in a mixed-strategy game , 2004, Nature Neuroscience.

[28]  Philip L. Smith,et al.  A comparison of sequential sampling models for two-choice reaction time. , 2004, Psychological review.

[29]  M. Platt,et al.  Risk-sensitive neurons in macaque posterior cingulate cortex , 2005, Nature Neuroscience.

[30]  Colin Camerer,et al.  Neural Systems Responding to Degrees of Uncertainty in Human Decision-Making , 2005, Science.

[31]  Angela J. Yu,et al.  Uncertainty, Neuromodulation, and Attention , 2005, Neuron.

[32]  P. Glimcher,et al.  JOURNAL OF THE EXPERIMENTAL ANALYSIS OF BEHAVIOR 2005, 84, 555–579 NUMBER 3(NOVEMBER) DYNAMIC RESPONSE-BY-RESPONSE MODELS OF MATCHING BEHAVIOR IN RHESUS MONKEYS , 2022 .

[33]  C. Padoa-Schioppa,et al.  Neurons in the orbitofrontal cortex encode economic value , 2006, Nature.

[34]  J. Hirsch,et al.  A Neural Representation of Categorization Uncertainty in the Human Brain , 2006, Neuron.

[35]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[36]  M. Quirk,et al.  Representation of Spatial Goals in Rat Orbitofrontal Cortex , 2006, Neuron.

[37]  M. Roesch,et al.  Encoding of Time-Discounted Rewards in Orbitofrontal Cortex Is Independent of Value Representation , 2006, Neuron.

[38]  Jonathan D. Cohen,et al.  The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. , 2006, Psychological review.

[39]  J. O'Doherty,et al.  Reward Value Coding Distinct From Risk Attitude-Related Uncertainty Coding in Human Reward Systems , 2006, Journal of neurophysiology.

[40]  J. Wallis Orbitofrontal cortex and its contribution to decision-making. , 2007, Annual review of neuroscience.

[41]  B. Richmond,et al.  A Comparison of Reward‐Contingent Neuronal Activity in Monkey Orbitofrontal Cortex and Ventral Striatum , 2007, Annals of the New York Academy of Sciences.

[42]  A. Cowey,et al.  Post-decision wagering objectively measures awareness , 2007, Nature Neuroscience.

[43]  C. Koch,et al.  Betting the house on consciousness , 2007, Nature Neuroscience.

[44]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[45]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[46]  J. Crystal,et al.  Metacognition in the Rat , 2007, Current Biology.