Matching Behavior and the Representation of Value in the Parietal Cortex

Sugrue, Leo P.; Corrado, Greg S.; Newsome, William T.

doi:10.1126/science.1094765

Cited by 1,030Neural and Behavioral Psychology StudiesDecision-Making and Behavioral EconomicsNeurotransmitter Receptor Influence on Behavior

Matching Behavior and the Representation of Value in the Parietal Cortex

Sugrue, Leo P., Corrado, Greg S., Newsome, William T.·2004·Science

DOI 10.1126/science.1094765

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Abstract

Psychologists and economists have long appreciated the contribution of reward history and expectation to decision-making. Yet we know little about how specific histories of choice and reward lead to an internal representation of the “value” of possible actions. We approached this problem through an integrated application of behavioral, computational, and physiological techniques. Monkeys were placed in a dynamic foraging environment in which they had to track the changing values of alternative choices through time. In this context, the monkeys' foraging behavior provided a window into their subjective valuation. We found that a simple model based on reward history can duplicate this behavior and that neurons in the parietal cortex represent the relative value of competing actions predicted by this model.

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LIP neurons are hypothesized to encode the attentional salience or expected value of a visual saccade target, but these concepts cannot explain the pattern of LIP activity in the experiment.
“LIP neurons are hypothesized to encode the attentional salience or expected value of a visual saccade target (52, 53, 63), but these concepts cannot explain the pattern of LIP activity in our experiment.”
From Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex (2009) · cites this paper as [52]
Previous studies have shown that LIP responses are modulated by many factors, such as attention, expectation, time, motor intention, experienced value, reward, and the prior probability of making an eye movement.
“In addition, previous studies have shown that LIP responses are modulated by many factors, such as attention, expectation, time, motor intention, experienced value, reward, and the prior probability of making an eye movement12,13,39–42.”
From Microstimulation of macaque area LIP affects decision-making in a motion discrimination task (2006) · cites this paper as [41]
In a dynamic payoff task, monkeys apportioned choices in proportion to recent reward history, and lateral intraparietal area neurons increased selective responses in proportion with the target's expected reward.
“Monkeys apportioned their choices in proportion to the recent history of rewards, and neurons in the lateral intraparietal area increased their selective responses in proportion with the target’s expected reward: firing for a saccade directed toward the receptive field increased monotonically (blue traces, dashed to solid), while firing for a saccade to a different location decreased monotonically”
From Attention, learning, and the value of information (2012) · cites this paper as Sugrue et al., 2004
Parietal neurons encoding target selection report an action value representation (the term V in Rescorla-Wagner) and update this representation dynamically.
“As described above, parietal neurons encoding target selection are thought to report an action value representation – the term V in the Rescorla-Wagner equation – and to update this representation in dynamic fashion (Sugrue et al., 2004).”
From Attention, learning, and the value of information (2012) · cites this paper as Sugrue et al., 2004
Similar results are obtained when target desirability is manipulated by relative magnitude, probability, or delay of expected reward.
“Similar results are obtained in tasks that manipulate the desirability of a target using different methods, for example by controlling the relative magnitude, probability or delay of its expected reward (Bernacchia et al., 2011; Louie et al., 2011; Sugrue et al., 2004; Yang and Shadlen, 2007).”
From Attention, learning, and the value of information (2012) · cites this paper as Sugrue et al., 2004

Single neurons in a number of cortical areas have activity correlated with reinforcer frequency and magnitude.
“Single neurons in a number of cortical areas have activity correlated with reinforcer frequency (Barraclough, Conroy, & Lee, 2004; Platt & Glimcher, 1999; Sugrue et al., 2004) and magnitude (Platt & Glimcher, 1999).”
From DYNAMIC RESPONSE-BY-RESPONSE MODELS OF MATCHING BEHAVIOR IN RHESUS MONKEYS (2005) · cites this paper as Sugrue et al., 2004
Dorris and Glimcher (2004) and Sugrue et al. (2004) found that activity of parietal cortex neurons was correlated with estimates of value derived by fitting models using reinforcement rate to predict monkeys' behavior.
“They found that the activity of neurons in parietal cortex was correlated with estimates of value derived by fitting models using reinforcement rate to predict the monkeys' behavior (similar to Figure 10, but without taking into account past choices).”
From DYNAMIC RESPONSE-BY-RESPONSE MODELS OF MATCHING BEHAVIOR IN RHESUS MONKEYS (2005) · cites this paper as Sugrue et al. (2004)
The decision behavior is influenced by past rewards harvested locally in time, in agreement with the observed monkey's behavior.
“Hence, the decision behavior is influenced by past rewards harvested locally in time, in agreement with the observed monkey’s behavior (Sugrue et al., 2004; Lau and Glimcher, 2005).”
From Decision Making in Recurrent Neuronal Circuits (2008) · cites this paper as Sugrue et al., 2004
Monkey's behavior conformed to the matching law, which states that a subject allocates her or his choices in a proportion which matches the relative reinforcement obtained from these choices.
“The studies found that monkey’s behavior conformed to the matching law, which states that a subject allocates her or his choices in a proportion which matches the relative reinforcement obtained from these choices (Herrnstein et al., 1997) (Figures 5A and 5B).”
From Decision Making in Recurrent Neuronal Circuits (2008) · cites this paper as Sugrue et al., 2004
Neural activity of LIP neurons selective for a saccadic response was modulated by a representation of the outcome value, defined behaviorally as a leaky integration of past rewards on that target.
“Moreover, neural activity of LIP neurons selective for a saccadic response was modulated by a representation of the outcome value, which was defined behaviorally as a leaky integration of past rewards on that target (Sugrue et al., 2004).”
From Decision Making in Recurrent Neuronal Circuits (2008) · cites this paper as Sugrue et al., 2004

Evolution and the theory of games
Smith, J. M. (1976) · Springer eBooks · doi:10.1007/978-1-4684-7862-4_22 · Cited by 7,369 · see citing works
Evolution and the Theory of Games
Smith, J. M. (1982) · Cambridge University Press eBooks · doi:10.1017/cbo9780511806292 · Cited by 6,918 · see citing works
Choices, values, and frames.
Kahneman, D., & Tversky, A. (1984) · American Psychologist · doi:10.1037/0003-066x.39.4.341 · Cited by 6,544 · see citing works
Computational modelling of visual attention
Itti, L., & Koch, C. (2001) · Nature Reviews Neuroscience · doi:10.1038/35058500 · Cited by 4,733 · see citing works
Shifts in Selective Visual Attention: Towards the Underlying Neural Circuitry
Christof Koch, A., & Ullman, S. (1987) · Springer eBooks · doi:10.1007/978-94-009-3833-5_5 · Cited by 3,739 · see citing works
Choices, Values, and Frames
(2000) · doi:10.1017/cbo9780511803475 · Cited by 2,987 · see citing works
Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex
Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. S. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.2.331 · Cited by 2,685 · see citing works
RELATIVE AND ABSOLUTE STRENGTH OF RESPONSE AS A FUNCTION OF FREQUENCY OF REINFORCEMENT 1, 2
Herrnstein, R. J. (1961) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1961.4-267 · Cited by 2,281 · see citing works
Neural Basis of a Perceptual Decision in the Parietal Cortex (Area LIP) of the Rhesus Monkey
Shadlen, M. N., & Newsome, W. T. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.4.1916 · Cited by 1,755 · see citing works
Self-citation
Neural correlates of decision variables in parietal cortex
Platt, M. L., & Glimcher, P. W. (1999) · Nature · doi:10.1038/22268 · Cited by 1,721 · see citing works
SPACE AND ATTENTION IN PARIETAL CORTEX
Colby, C. L., & Goldberg, M. E. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.319 · Cited by 1,710 · see citing works
Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task
Roitman, J. D., & Shadlen, M. N. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-21-09475.2002 · Cited by 1,589 · see citing works
The representation of visual salience in monkey parietal cortex
Gottlieb, J. P., Kusunoki, M., & Goldberg, M. E. (1998) · Nature · doi:10.1038/35135 · Cited by 1,078 · see citing works
Memory related motor planning activity in posterior parietal cortex of macaque
Gnadt, J. W., & Andersen, R. A. (1988) · Experimental Brain Research · doi:10.1007/bf00271862 · Cited by 998 · see citing works
Neural computations that underlie decisions about sensory stimuli
Gold, J. I., & Shadlen, M. N. (2001) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01567-9 · Cited by 881 · see citing works
Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention
Bisley, J. W., & Goldberg, M. E. (2003) · Science · doi:10.1126/science.1077395 · Cited by 821 · see citing works
Motion perception: seeing and deciding.
Shadlen, M. N., & Newsome, W. T. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.2.628 · Cited by 723 · see citing works
Self-citation
Prefrontal cortex and decision making in a mixed-strategy game
Barraclough, D. J., Conroy, M. L., & Lee, D. (2004) · Nature Neuroscience · doi:10.1038/nn1209 · Cited by 678 · see citing works
The Matching Law: A Research Review
Davison, M., & McCarthy, D. (2016) · Medical Entomology and Zoology · Cited by 667 · see citing works
Ecology an Evolutionary Approach
Emlen, J. M. (1973) · Andalas University Repository (Andalas University) · Cited by 578 · see citing works
Limits to Action: The Allocation of Individual Behavior
Baum, W. E., & Staddon, J. E. R. (1982) · The American Journal of Psychology · doi:10.2307/1422478 · Cited by 557 · see citing works
Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology
Schultz, W. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.017 · Cited by 517 · see citing works
Learning the evolutionarily stable strategy
Harley, C. B. (1981) · Journal of Theoretical Biology · doi:10.1016/0022-5193(81)90032-1 · Cited by 358 · see citing works
Toward a law of response strength.
de Villiers, P. A., & Herrnstein, R. J. (1976) · Psychological Bulletin · doi:10.1037/0033-2909.83.6.1131 · Cited by 279 · see citing works
OPTIMIZATION AND THE MATCHING LAW AS ACCOUNTS OF INSTRUMENTAL BEHAVIOR
Baum, W. M. (1981) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1981.36-387 · Cited by 249 · see citing works
The rat approximates an ideal detector of changes in rates of reward: Implications for the law of effect.
Gallistel, C. R., Mark, T. A., King, A. P., & Latham, P. E. (2001) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.27.4.354 · Cited by 225 · see citing works
CHOICE IN A VARIABLE ENVIRONMENT: EVERY REINFORCER COUNTS
Davison, M., & Baum, W. M. (2000) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.2000.74-1 · Cited by 214 · see citing works
The rat approximates an ideal detector of changes in rates of reward: Implications for the law of effect.
Gallistel, C. R., Mark, T. A., King, A. P., et al. (2001) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.27.4.354 · Cited by 174 · see citing works
On matching and maximizing in operant choice experiments.
Staddon, J. E. R., & Motheral, S. (1978) · Psychological Review · doi:10.1037/0033-295x.85.5.436 · Cited by 159 · see citing works
A MARKOV MODEL DESCRIPTION OF CHANGEOVER PROBABILITIES ON CONCURRENT VARIABLE‐INTERVAL SCHEDULES1
Heyman, G. M. (1979) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1979.31-41 · Cited by 122 · see citing works
Melioration: A Theory of Distributed Choice
Herrnstein, R., & Prélec, D. (1991) · The Journal of Economic Perspectives · doi:10.1257/jep.5.3.137 · Cited by 72 · see citing works

Flagged first, then by citations

Sorted by citations

The Neural Basis of Decision Making
Gold, J. I., & Shadlen, M. N. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.113038 · Cited by 3,764 · see citing works
Cortical substrates for exploratory decisions in humans
Daw, N. D., O'Doherty, J. P., Dayan, P., Seymour, B., & Dolan, R. J. (2006) · Nature · doi:10.1038/nature04766 · Cited by 2,224 · see citing works
Learning the value of information in an uncertain world
Behrens, T. E. J., Woolrich, M. W., Walton, M. E., & Rushworth, M. F. S. (2007) · Nature Neuroscience · doi:10.1038/nn1954 · Cited by 2,053 · see citing works
The neural correlates of subjective value during intertemporal choice
Kable, J. W., & Glimcher, P. W. (2007) · Nature Neuroscience · doi:10.1038/nn2007 · Cited by 1,916 · see citing works
Habits, Rituals, and the Evaluative Brain
Graybiel, A. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112851 · Cited by 1,697 · see citing works
Top-down versus bottom-up attentional control: a failed theoretical dichotomy
Awh, E., Belopolsky, A. V., & Theeuwes, J. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.06.010 · Cited by 1,557 · see citing works
Behavioral Theories and the Neurophysiology of Reward
Schultz, W. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070229 · Cited by 1,637 · see citing works
Toward a second-person neuroscience
Schilbach, L., Timmermans, B., Reddy, V., Costall, A., Bente, G., Schlicht, T., & Vogeley, K. (2013) · Behavioral and Brain Sciences · doi:10.1017/s0140525x12000660 · Cited by 1,510 · see citing works
Neural Mechanisms for Interacting with a World Full of Action Choices
Cisek, P., & Kalaska, J. F. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135409 · Cited by 1,543 · see citing works
Neuronal Reward and Decision Signals: From Theories to Data
Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126 · see citing works
States versus Rewards: Dissociable Neural Prediction Error Signals Underlying Model-Based and Model-Free Reinforcement Learning
Gläscher, J., Daw, N., Dayan, P., & O'Doherty, J. P. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.016 · Cited by 1,166 · see citing works
Should I stay or should I go? How the human brain manages the trade-off between exploitation and exploration
Cohen, J. D., McClure, S. M., & Yu, A. J. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2098 · Cited by 1,121 · see citing works
Stimulus onset quenches neural variability: A widespread cortical phenomenon
Churchland, M. M., Yu, B. M., Cunningham, J. P., Sugrue, L. P., Cohen, M. R., Corrado, G. S., Newsome, W. T., Clark, A. M., Hosseini, P., Scott, B. B., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2501 · Cited by 1,084 · see citing works
Self-citation
Attention, intention, and priority in the parietal lobe
Bisley, J. W., & Goldberg, M. E. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-152823 · Cited by 1,043 · see citing works
Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex
Kiani, R., & Shadlen, M. N. (2009) · Science · doi:10.1126/science.1169405 · Cited by 1,027 · see citing works
Optimal decision making and the anterior cingulate cortex
Kennerley, S. W., Walton, M. E., Behrens, T. E. J., Buckley, M. J., & Rushworth, M. F. S. (2006) · Nature Neuroscience · doi:10.1038/nn1724 · Cited by 948 · see citing works
The Neurobiology of Decision: Consensus and Controversy
Kable, J. W., & Glimcher, P. W. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.003 · Cited by 928 · see citing works
Learned predictions of error likelihood in the anterior cingulate cortex
Brown, J. W., & Braver, T. S. (2005) · Science · doi:10.1126/science.1105783 · Cited by 928 · see citing works
Neural correlates, computation and behavioural impact of decision confidence
Kepecs, A., Uchida, N., Zariwala, H. A., & Mainen, Z. F. (2008) · Nature · doi:10.1038/nature07200 · Cited by 809 · see citing works
Choice, uncertainty and value in prefrontal and cingulate cortex
Rushworth, M. F. S., & Behrens, T. E. J. (2008) · Nature Neuroscience · doi:10.1038/nn2066 · Cited by 866 · see citing works
Eye guidance in natural vision: reinterpreting salience
Tatler, B. W., Hayhoe, M. M., Land, M. F., & Ballard, D. H. (2011) · Journal of Vision · doi:10.1167/11.5.5 · Cited by 775 · see citing works
A general mechanism for perceptual decision-making in the human brain
Heekeren, H. R., Marrett, S., Bandettini, P. A., & Ungerleider, L. G. (2004) · Nature · doi:10.1038/nature02966 · Cited by 741 · see citing works
Probabilistic population codes for Bayesian decision making
Beck, J. M., Ma, W. J., Kiani, R., Hanks, T., Churchland, A. K., Roitman, J., Shadlen, M. N., Latham, P. E., & Pouget, A. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.021 · Cited by 645 · see citing works
Decision Making in Recurrent Neuronal Circuits
Wang, X.-J. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.034 · Cited by 679 · see citing works
“(A) is reproduced with permission from Sugrue et al. (2004), (B) and (C) from Corrado et al. (2005), and (D)–(G) from Soltani and Wang (2006). of fluctuating network dynamics (Soltani and Wang, 2006).”
BackgroundResultInfluential
Modulators of decision making
Doya, K. (2008) · Nature Neuroscience · doi:10.1038/nn2077 · Cited by 642 · see citing works
Slow cortical dynamics and the accumulation of information over long timescales
Honey, C. J., Thesen, T., Donner, T. H., Silbert, L. J., Carlson, C. E., Devinsky, O., Doyle, W. K., Rubin, N., Heeger, D. J., & Hasson, U. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.011 · Cited by 532 · see citing works
Neurobiology of economic choice: a good-based model
Padoa-Schioppa, C. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113648 · Cited by 600 · see citing works
An event-related functional magnetic resonance imaging study of voluntary and stimulus-driven orienting of attention
Kincade, J. M., Abrams, R. A., Astafiev, S. V., Shulman, G. L., & Corbetta, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0236-05.2005 · Cited by 561 · see citing works
Representation of negative motivational value in the primate lateral habenula
Matsumoto, M., & Hikosaka, O. (2009) · Nature Neuroscience · doi:10.1038/nn.2233 · Cited by 547 · see citing works
Experience-dependent representation of visual categories in parietal cortex
Freedman, D. J., & Assad, J. A. (2006) · Nature · doi:10.1038/nature05078 · Cited by 542 · see citing works
Neural Activity in Macaque Parietal Cortex Reflects Temporal Integration of Visual Motion Signals during Perceptual Decision Making
Huk, A. C., & Shadlen, M. N. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4684-04.2005 · Cited by 538 · see citing works
Choosing the greater of two goods: neural currencies for valuation and decision making
Sugrue, L. P., Corrado, G. S., & Newsome, W. T. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1666 · Cited by 536 · see citing works
Self-citation
The role of the ventromedial prefrontal cortex in abstract state-based inference during decision making in humans
Hampton, A. N., Bossaerts, P., & O’Doherty, J. P. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1010-06.2006 · Cited by 498 · see citing works
Midbrain dopamine neurons encode decisions for future action
Morris, G., Nevet, A., Arkadir, D., Vaadia, E., & Bergman, H. (2006) · Nature Neuroscience · doi:10.1038/nn1743 · Cited by 503 · see citing works
DYNAMIC RESPONSE-BY-RESPONSE MODELS OF MATCHING BEHAVIOR IN RHESUS MONKEYS
Lau, B., & Glimcher, P. W. (2005) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.2005.110-04 · Cited by 485 · see citing works
Mechanisms underlying cortical activity during value-guided choice
Hunt, L. T., Kolling, N., Soltani, A., Woolrich, M. W., Rushworth, M. F. S., & Behrens, T. E. J. (2012) · Nature Neuroscience · doi:10.1038/nn.3017 · Cited by 454 · see citing works
Neurons in the frontal lobe encode the value of multiple decision variables
Kennerley, S. W., Dahmubed, A. F., Lara, A. H., & Wallis, J. D. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21100 · Cited by 453 · see citing works
Elapsed Decision Time Affects the Weighting of Prior Probability in a Perceptual Decision Task
Hanks, T. D., Mazurek, M. E., Kiani, R., Hopp, E., & Shadlen, M. N. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5613-10.2011 · Cited by 378 · see citing works
Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making
Gläscher, J., Hampton, A. N., & O'Doherty, J. P. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn098 · Cited by 387 · see citing works
Modulation of visual processing by attention and emotion: Windows on causal interactions between human brain regions
Vuilleumier, P., & Driver, J. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2092 · Cited by 397 · see citing works
Basal ganglia orient eyes to reward
Hikosaka, O., Nakamura, K., & Nakahara, H. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00458.2005 · Cited by 377 · see citing works
Selection history: How reward modulates selectivity of visual attention.
Failing, M., & Theeuwes, J. (2018) · Psychonomic Bulletin & Review · doi:10.3758/s13423-017-1380-y · Cited by 345 · see citing works
Frontal cortex subregions play distinct roles in choices between actions and stimuli
Rudebeck, P. H., Behrens, T. E., Kennerley, S. W., Baxter, M. G., Buckley, M. J., Walton, M. E., & Rushworth, M. F. S. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3541-08.2008 · Cited by 350 · see citing works
Microstimulation of macaque area LIP affects decision-making in a motion discrimination task
Hanks, T. D., Ditterich, J., & Shadlen, M. N. (2006) · Nature Neuroscience · doi:10.1038/nn1683 · Cited by 360 · see citing works
Rewards teach visual selective attention
Chelazzi, L., Perlato, A., Santandrea, E., & Della Libera, C. (2013) · Vision Research · doi:10.1016/j.visres.2012.12.005 · Cited by 354 · see citing works
Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala
Belova, M. A., Paton, J. J., Morrison, S. E., & Salzman, C. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.004 · Cited by 349 · see citing works
A computational framework for the study of confidence in humans and animals
Kepecs, A., & Mainen, Z. F. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0037 · Cited by 305 · see citing works
Integrated neural processes for defining potential actions and deciding between them: a computational model
Cisek, P. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.5605-05.2006 · Cited by 344 · see citing works
Learning to Attend and to Ignore Is a Matter of Gains and Losses
Della Libera, C., & Chelazzi, L. (2009) · Psychological Science · doi:10.1111/j.1467-9280.2009.02360.x · Cited by 329 · see citing works
Temporal Filtering of Reward Signals in the Dorsal Anterior Cingulate Cortex during a Mixed-Strategy Game
Seo, H., & Lee, D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2369-07.2007 · Cited by 324 · see citing works
An “As Soon As Possible” Effect in Human Intertemporal Decision Making: Behavioral Evidence and Neural Mechanisms
Kable, J. W., & Glimcher, P. W. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00177.2009 · Cited by 316 · see citing works
Reward value-based gain control: divisive normalization in parietal cortex
Louie, K., Grattan, L. E., & Glimcher, P. W. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1237-11.2011 · Cited by 308 · see citing works
“Previous studies have framed LIP activity in terms of gain ratio (Platt and Glimcher, 1999) or fractional income (Sugrue et al., 2004; Corrado et al., 2005), both of which assume a fractional reward representation based on V in / (Vin Vout), but no study has isolated the effect of manipulating…”
BackgroundResultInfluential
Bayesian Spiking Neurons I: Inference
Deneve, S. (2008) · Neural Computation · doi:10.1162/neco.2008.20.1.91 · Cited by 313 · see citing works
Immediate Reward Bias in Humans: Fronto-Parietal Networks and a Role for the Catechol-O-Methyltransferase 158Val/ValGenotype
Boettiger, C. A., Mitchell, J. M., Tavares, V. C., Robertson, M., Joslyn, G., D'Esposito, M., & Fields, H. L. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2551-07.2007 · Cited by 300 · see citing works
Neural computations underlying action-based decision making in the human brain
Wunderlich, K., Rangel, A., & O'Doherty, J. P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901077106 · Cited by 301 · see citing works
Combined effects of attention and motivation on visual task performance: Transient and sustained motivational effects
Engelmann, J. B. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.004.2009 · Cited by 300 · see citing works
Neural Coding of Uncertainty and Probability
Ma, W. J., & Jazayeri, M. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071013-014017 · Cited by 290 · see citing works
The Role of Human Orbitofrontal Cortex in Value Comparison for Incommensurable Objects
FitzGerald, T. H. B., Seymour, B., & Dolan, R. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0717-09.2009 · Cited by 279 · see citing works
Dopamine modulates novelty seeking behavior during decision making.
Costa, V. D., Tran, V. L., Turchi, J., & Averbeck, B. B. (2014) · Behavioral Neuroscience · doi:10.1037/a0037128 · Cited by 263 · see citing works
Dopamine prediction error responses integrate subjective value from different reward dimensions
Lak, A., Stauffer, W. R., & Schultz, W. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1321596111 · Cited by 257 · see citing works
Attention, learning, and the value of information
Gottlieb, J. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.034 · Cited by 241 · see citing works
“Reproduced with permission from Sugrue et al. (2004).”
BackgroundResultInfluential
Moment-to-moment tracking of state value in the amygdala
Belova, M. A., Paton, J. J., & Salzman, C. D. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1400-08.2008 · Cited by 221 · see citing works
Perceptual decision making in less than 30 milliseconds
Stanford, T. R., Shankar, S., Massoglia, D. P., Costello, M. G., & Salinas, E. (2010) · Nature Neuroscience · doi:10.1038/nn.2485 · Cited by 228 · see citing works
Reward modulates attention independently of action value in posterior parietal cortex
Peck, C. J., Jangraw, D. C., Suzuki, M., Efem, R., & Gottlieb, J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1929-09.2009 · Cited by 219 · see citing works
Contributions of the ventromedial prefrontal cortex to goal-directed action selection
O’Doherty, J. P. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06290.x · Cited by 225 · see citing works
Motivation sharpens exogenous spatial attention.
Engelmann, J. B., & Pessoa, L. (2007) · Emotion · doi:10.1037/1528-3542.7.3.668 · Cited by 221 · see citing works
Neural Mechanisms of Belief Inference during Cooperative Games
Yoshida, W., Seymour, B., Friston, K. J., & Dolan, R. J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5895-09.2010 · Cited by 212 · see citing works
A neural mechanism for sensing and reproducing a time interval
Jazayeri, M., & Shadlen, M. N. (2015) · Current Biology · doi:10.1016/j.cub.2015.08.038 · Cited by 210 · see citing works
LINEAR-NONLINEAR-POISSON MODELS OF PRIMATE CHOICE DYNAMICS
Corrado, G. S., Sugrue, L. P., Seung, H. S., & Newsome, W. T. (2005) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.2005.23-05 · Cited by 206 · see citing works
Self-citation
Altering Spatial Priority Maps via Reward-Based Learning
Chelazzi, L., E to inova, J., Calletti, R., Lo Gerfo, E., Sani, I., Della Libera, C., & Santandrea, E. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0277-14.2014 · Cited by 195 · see citing works
A neural circuit model of flexible sensorimotor mapping: learning and forgetting on multiple timescales
Fusi, S., Asaad, W. F., Miller, E. K., & Wang, X.-J. (2007) · Neuron · doi:10.1016/j.neuron.2007.03.017 · Cited by 199 · see citing works
Beyond working memory: the role of persistent activity in decision making
Curtis, C. E., & Lee, D. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.03.006 · Cited by 191 · see citing works
Serotonin neurons modulate learning rate through uncertainty
Grossman, C. D., Bari, B. A., & Cohen, J. Y. (2022) · Current Biology · doi:10.1016/j.cub.2021.12.006 · Cited by 164 · see citing works
Bayesian sampling in visual perception
Moreno-Bote, R., Knill, D. C., & Pouget, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101430108 · Cited by 182 · see citing works
Building Bridges between Perceptual and Economic Decision-Making: Neural and Computational Mechanisms
Summerfield, C., & Tsetsos, K. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00070 · Cited by 167 · see citing works
Stable representations of decision variables for flexible behavior
Bari, B. A., Grossman, C. D., Lubin, E. E., Rajagopalan, A. E., Cressy, J. I., & Cohen, J. Y. (2019) · Neuron · doi:10.1016/j.neuron.2019.06.001 · Cited by 173 · see citing works
Orbitofrontal contributions to value-based decision making: evidence from humans with frontal lobe damage
Fellows, L. K. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06229.x · Cited by 169 · see citing works
A unified selection signal for attention and reward in primary visual cortex
Stănişor, L., van der Togt, C., Pennartz, C. M. A., & Roelfsema, P. R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300117110 · Cited by 158 · see citing works
Reinforcement learning and decision making in monkeys during a competitive game
Lee, D., Conroy, M. L., McGreevy, B. P., & Barraclough, D. J. (2004) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2004.07.007 · Cited by 156 · see citing works
Influence of history on saccade countermanding performance in humans and macaque monkeys
Emeric, E. E., Brown, J. W., Boucher, L., Carpenter, R. H. S., Hanes, D. P., Harris, R., Logan, G. D., Mashru, R. N., Paré, M., Pouget, P., et al. (2007) · Vision Research · doi:10.1016/j.visres.2006.08.032 · Cited by 151 · see citing works
One-dimensional dynamics of attention and decision making in LIP
Ganguli, S., Bisley, J. W., Roitman, J. D., Shadlen, M. N., Goldberg, M. E., & Miller, K. D. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.038 · Cited by 152 · see citing works
The why, what, where, when and how of goal-directed choice: neuronal and computational principles
Verschure, P. F. M. J., Pennartz, C. M. A., & Pezzulo, G. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0483 · Cited by 131 · see citing works
“Even structures such as posterior parietal cortex and primary sensory cortex (A1, V1) are deeply affected by associative stimulus–reward and action–reward learning [56–62].”
BackgroundMethod
Lateral Intraparietal Cortex and Reinforcement Learning during a Mixed-Strategy Game
Seo, H., Barraclough, D. J., & Lee, D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1479-09.2009 · Cited by 125 · see citing works
Functional neuroimaging of intertemporal choice models: a review
Carter, R. M., Meyer, J. R., & Huettel, S. A. (2010) · Journal of Neuroscience Psychology and Economics · doi:10.1037/a0018046 · Cited by 124 · see citing works
Generalization of value in reinforcement learning by humans
Wimmer, G. E., Daw, N. D., & Shohamy, D. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08017.x · Cited by 111 · see citing works
Human reinforcement learning subdivides structured action spaces by learning effector-specific values
Gershman, S. J., Pesaran, B., & Daw, N. D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2469-09.2009 · Cited by 118 · see citing works
An effect of serotonergic stimulation on learning rates for rewards apparent after long intertrial intervals
Iigaya, K., Fonseca, M. S., Murakami, M., Mainen, Z. F., & Dayan, P. (2018) · Nature Communications · doi:10.1038/s41467-018-04840-2 · Cited by 120 · see citing works
Reward facilitates tactile judgments and modulates hemodynamic responses in human primary somatosensory cortex
Pleger, B., Blankenburg, F., Ruff, C. C., Driver, J., & Dolan, R. J. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1093-08.2008 · Cited by 120 · see citing works
Reinforcement learning: Computational theory and biological mechanisms
Doya, K. (2007) · HFSP journal · doi:10.2976/1.2732246 · Cited by 150 · see citing works
The case against economic values in the orbitofrontal cortex (or anywhere else in the brain).
Hayden, B. Y., & Niv, Y. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000448 · Cited by 127 · see citing works
Encoding of both positive and negative reward prediction errors by neurons of the primate lateral prefrontal cortex and caudate nucleus
Asaad, W. F., & Eskandar, E. N. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3793-11.2011 · Cited by 105 · see citing works
Neuronal correlates of the set-size effect in monkey lateral intraparietal area
Balan, P. F., Oristaglio, J., Schneider, D. M., & Gottlieb, J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060158 · Cited by 83 · see citing works
Neural mechanism for stochastic behaviour during a competitive game
Soltani, A., Lee, D., & Wang, X.-J. (2006) · Neural Networks · doi:10.1016/j.neunet.2006.05.044 · Cited by 77 · see citing works
Distinct roles for the amygdala and orbitofrontal cortex in representing the relative amount of expected reward
Saez, R. A., Saez, A., Paton, J. J., Lau, B., & Salzman, C. D. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.012 · Cited by 75 · see citing works
Reward-Based Transfer From Bottom-Up to Top-Down Search Tasks
Lee, J., & Shomstein, S. (2014) · Psychological Science · doi:10.1177/0956797613509284 · Cited by 70 · see citing works
Action-specific value signals in reward-related regions of the human brain
FitzGerald, T. H. B., Friston, K. J., & Dolan, R. J. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3254-12.2012 · Cited by 68 · see citing works
The Role of the Parietal Cortex in the Representation of Task-Reward Associations
Wisniewski, D., Reverberi, C., Momennejad, I., Kahnt, T., & Haynes, J.-D. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4882-14.2015 · Cited by 67 · see citing works
Valuation of uncertain and delayed rewards in primate prefrontal cortex
Kim, S., Hwang, J., Seo, H., & Lee, D. (2009) · Neural Networks · doi:10.1016/j.neunet.2009.03.010 · Cited by 37 · see citing works
Rational thoughts in neural codes
Wu, Z., Kwon, M., Daptardar, S., Schrater, P., & Pitkow, X. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1912336117 · Cited by 27 · see citing works
Reward-based plasticity of spatial priority maps: Exploiting inter-subject variability to probe the underlying neurobiology
Della Libera, C., Calletti, R., Eštočinová, J., Chelazzi, L., & Santandrea, E. (2017) · Cognitive Neuroscience · doi:10.1080/17588928.2016.1213226 · Cited by 11 · see citing works

Differential time allocation of foraging workers in the subterranean termite
Lee, S., Chouvenc, T., & Su, N. (2021) · Frontiers in Zoology · doi:10.1186/s12983-021-00446-5 · Cited by 18 · see citing works
Individual foraging in the antPachycondyla apicalis
Goss, S., Fresneau, D., Deneubourg, J. L., et al. (1989) · Oecologia · doi:10.1007/bf00789933 · Cited by 19 · see citing works
Foraging ecology of the thermophilic Australian desert ant, Melophorus bagoti
Muser, B., Sommer, S., Wolf, H., et al. (2005) · Australian Journal of Zoology · doi:10.1071/zo05023 · Cited by 107 · see citing works
Effect of conspecific neighbors on the foraging activity levels of the wintering Oriental Storks (Ciconia boyciana): Benefits of social information
Cheng, L., Zhou, L., Bao, Y., et al. (2020) · Ecology and Evolution · doi:10.1002/ece3.6693 · Cited by 10 · see citing works
South for the winter? Within‐dive foraging effort reveals the trade‐offs between divergent foraging strategies in a free‐ranging predator
Arthur, B., Hindell, M. A., Bester, M. N., Oosthuizen, W. C., Wege, M., & Lea, M. (2016) · Functional Ecology · doi:10.1111/1365-2435.12636 · Cited by 37 · see citing works

Authors: Sugrue, L. P., Corrado, G. S., & Newsome, W. T.
Affiliations: Howard Hughes Medical Institute (US)
Corresponding author: Sugrue, Leo P.
ORCID: Sugrue, Leo P.
Corrado, Greg S.
Newsome, William T.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2004-06-18
Volume: 304
Issue: 5678
Pages: 1782-1787
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1094765
OpenAlex: W2019310225
Semantic Scholar: 2ed6866784ae093c3a2a6cb9f8c7b8a11076ca0e
Cited by: 1,030
References: 31
Citations by year: 2026: 22 · 2025: 21 · 2024: 27 · 2023: 29 · 2022: 34 · 2021: 34 · 2020: 31 · 2019: 43 · 2018: 29 · 2017: 34 · 2016: 38 · 2015: 51 · 2014: 58 · 2013: 59 · 2012: 59
FWCI: 29.38
Type: journal article
Language: en
Open access: closed
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Social Sciences › Decision Sciences › General Decision Sciences › Decision-Making and Behavioral Economics
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: value representation, parietal cortex, reward history, subjective value, foraging behavior, decision-making, reward anticipation
MeSH terms: Animals, Brain Mapping, Choice Behavior, Computer Simulation, Cues, Decision Making, Macaca mulatta, Male, Mathematics, Models, Psychological, Neurons, Parietal Lobe, Probability, Regression Analysis, Reward, Saccades

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Matching Behavior and the Representation of Value in the Parietal Cortex

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