Neuronal representations of cognitive state: reward or attention?
Abstract
The effects of spatial or featural attention on the activity of neurons have been studied in many experiments that have used a variety of neurophysiological approaches. Other experiments have examined how expectations about reward are represented in neuronal activity in various brain regions. Although attention and reward are distinct concepts, I argue here that many neurophysiological experiments on attention and reward do not permit a clean dissociation between the two. This problem arises in part because reward contingencies are the only parameter manipulated in any of these experiments. I describe how attention and reward expectations have been confounded, giving rise to uncertainty about how signals related to attention and reward are distributed in the brain.
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Reward automatically changes the visual salience of reward-associated perceptual features, and this is theoretically distinct from the known role of reward in the strategic establishment of attentional set.
“The direct nature of this influence deserves emphasis; the idea is that reward automatically changes the visual salience of reward-associated perceptual features, and this is theoretically distinct from the known role of reward in the strategic establishmentofattentional set (Maunsell, 2004).”
From Reward Changes Salience in Human Vision via the Anterior Cingulate (2010) · cites this paper as Maunsell, 2004
Irrespective of whether reward was signaled prior to a block of trials, prior to an individual trial, or contingent on the target, the beneficial influence of reward in these studies can be readily explained in terms of ongoing top-down attentional control processes.
“Irrespective of whether reward was signaled prior to a block of trials, prior to an individual trial, or contingent on the target, the beneficial influence of reward in all these studies can be readily explained in terms of ongoing top-down attentional control processes (Maunsell, 2004; Stănişor, van der Togt, Pennartz, & Roelfsema, 2013).”
From Selection history: How reward modulates selectivity of visual attention. (2018) · cites this paper as Maunsell, 2004
Cites
Posner, M. I. (1980) · Quarterly Journal of Experimental Psychology · doi:10.1080/00335558008248231 · Cited by 9,670 · 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
Food reward: brain substrates of wanting and liking
Berridge, K. C. (1996) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00033-b · Cited by 1,901 · see citing works
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
Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex
Luck, S. J., Chelazzi, L., Hillyard, S. A., & Desimone, R. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.1.24 · Cited by 1,615 · see citing works
Pashler, H. (1997) · doi:10.7551/mitpress/5677.001.0001 · Cited by 1,607 · see citing works
Feature-based attention influences motion processing gain in macaque visual cortex
Treue, S., & Trujillo, J. C. M. (1999) · Nature · doi:10.1038/21176 · Cited by 1,465 · see citing works
Multiple reward signals in the brain
Schultz, W. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044563 · Cited by 1,303 · see citing works
Neural responses during anticipation of a primary taste reward
O'Doherty, J. P., Deichmann, R., Critchley, H. D., & Dolan, R. J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00603-7 · Cited by 1,076 · see citing works
Increased Attention Enhances Both Behavioral and Neuronal Performance
Spitzer, H., Desimone, R., & Moran, J. (1988) · Science · doi:10.1126/science.3353728 · Cited by 815 · see citing works
Responses of Neurons in Inferior Temporal Cortex During Memory-Guided Visual Search
Chelazzi, L., Duncan, J., Miller, E. K., & Desimone, R. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.6.2918 · Cited by 726 · see citing works
Reward expectancy in primate prefrental neurons
Watanabe, M. (1996) · Nature · doi:10.1038/382629a0 · Cited by 684 · see citing works
Expectation of reward modulates cognitive signals in the basal ganglia
Kawagoe, R., Takikawa, Y., & Hikosaka, O. (1998) · Nature Neuroscience · doi:10.1038/1625 · Cited by 632 · see citing works
Modulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability
Basso, M. A., & Wurtz, R. H. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07519.1998 · Cited by 474 · see citing works
Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task
Fuster, J. M., & Jervey, J. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-03-00361.1982 · Cited by 463 · see citing works
Leon, M. I., & Shadlen, M. N. (1999) · Neuron · doi:10.1016/s0896-6273(00)80854-5 · Cited by 449 · see citing works
Neural correlates of attention in primate visual cortex
Treue, S. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01814-2 · Cited by 433 · see citing works
A neural correlate of response bias in monkey caudate nucleus
Lauwereyns, J., Watanabe, K., Coe, B. C., & Hikosaka, O. (2002) · Nature · doi:10.1038/nature00892 · Cited by 415 · see citing works
Saccadic Probability Influences Motor Preparation Signals and Time to Saccadic Initiation
Dorris, M. C., & Munoz, D. P. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-17-07015.1998 · Cited by 399 · see citing works
Influence of Reward Expectation on Behavior-Related Neuronal Activity in Primate Striatum
Hollerman, J. R., Tremblay, L., & Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.2.947 · Cited by 380 · see citing works
Modulation of neuronal activity by target uncertainty
Basso, M. A., & Wurtz, R. H. (1997) · Nature · doi:10.1038/37975 · Cited by 359 · see citing works
Attention to Both Space and Feature Modulates Neuronal Responses in Macaque Area V4
McAdams, C. J., & Maunsell, J. H. R. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.3.1751 · Cited by 343 · see citing works
Self-citationCortical mechanisms of space-based and object-based attentional control
Yantis, S., & Serences, J. T. (2003) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(03)00033-3 · Cited by 342 · see citing works
Roesch, M. R., & Olson, C. R. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00019.2003 · Cited by 309 · see citing works
Reward-Dependent Gain and Bias of Visual Responses in Primate Superior Colliculus
Ikeda, T., & Hikosaka, O. (2003) · Neuron · doi:10.1016/s0896-6273(03)00464-1 · Cited by 233 · see citing works
The role of attention in visual processing
Maunsell, J. H. R., & Cook, E. P. (2002) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1107 · Cited by 214 · see citing works
Self-citationDissociation of visual, motor and predictive signals in parietal cortex during visual guidance
Eskandar, E. N., & Assad, J. A. (1999) · Nature Neuroscience · doi:10.1038/4594 · Cited by 212 · see citing works
Influence of Reward Expectation on Visuospatial Processing in Macaque Lateral Prefrontal Cortex
Kobayashi, S., Lauwereyns, J., Koizumi, M., Sakagami, M., & Hikosaka, O. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00472.2001 · Cited by 206 · see citing works
Responses of Intraparietal Neurons to Saccadic Targets and Visual Distractors
Platt, M. L., & Glimcher, P. W. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.3.1574 · Cited by 194 · see citing works
Conceptual issues related to the role of the superior colliculus in the control of gaze
Sparks, D. L. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00039-2 · Cited by 193 · see citing works
Role of Primate Substantia Nigra Pars Reticulata in Reward-Oriented Saccadic Eye Movement
Sato, M., & Hikosaka, O. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-06-02363.2002 · Cited by 191 · see citing works
Prefrontal unit activity during associative learning in the monkey
Watanabe, M. (1990) · Experimental Brain Research · doi:10.1007/bf00228157 · Cited by 149 · see citing works
Feature-Based Anticipation of Cues that Predict Reward in Monkey Caudate Nucleus
Lauwereyns, J., Takikawa, Y., Kawagoe, R., Kobayashi, S., Koizumi, M., Coe, B. C., Sakagami, M., & Hikosaka, O. (2002) · Neuron · doi:10.1016/s0896-6273(02)00571-8 · Cited by 123 · see citing works
Neural Correlates of Rewarded and Unrewarded Eye Movements in the Primate Caudate Nucleus
Watanabe, K., Lauwereyns, J., & Hikosaka, O. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-31-10052.2003 · Cited by 118 · see citing works
Powell, K. D., & Goldberg, M. E. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.1.301 · Cited by 111 · see citing works
Instructed Delay Activity in the Human Prefrontal Cortex is Modulated by Monetary Reward Expectation
Ramnani, N. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.3.318 · Cited by 91 · see citing works
Spitzer, H., & Richmond, B. J. (1991) · Experimental Brain Research · doi:10.1007/bf00231157 · Cited by 83 · see citing works
Object-based vision and attention in primates
Olson, C. R. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00193-8 · Cited by 71 · see citing works
Motivation focuses attention and enhances neuronal selectivity in parietal cortex
Bendiksby, M. S., Jarman, A. F., & Platt, M. L. (2004) · Journal of Vision · doi:10.1167/4.8.624 · Cited by 4 · see citing works
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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
A taxonomy of external and internal attention.
Chun, M. M., Golomb, J. D., & Turk-Browne, N. B. (2011) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100427 · Cited by 1,472 · see citing works
Value-driven attentional capture
Anderson, B. A., Laurent, P. A., & Yantis, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104047108 · Cited by 1,098 · see citing works
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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
Reward Changes Salience in Human Vision via the Anterior Cingulate
Hickey, C., Chelazzi, L., & Theeuwes, J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1026-10.2010 · Cited by 606 · see citing works
“The direct nature of this influence deserves emphasis; the idea is that reward automatically changes the visual salience of reward-associated perceptual features, and this is theoretically distinct from the known role of reward in the strategic establishment of attentional set (Maunsell, 2004).”
BackgroundNeurobiology 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
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Sarter, M., Gehring, W. J., & Kozak, R. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2005.11.002 · Cited by 552 · see citing works
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Sugrue, L. P., Corrado, G. S., & Newsome, W. T. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1666 · Cited by 536 · see citing works
What the orbitofrontal cortex does not do
Stalnaker, T. A., Cooch, N. K., & Schoenbaum, G. (2015) · Nature Neuroscience · doi:10.1038/nn.3982 · Cited by 531 · see citing works
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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
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
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Hikosaka, O., Nakamura, K., & Nakahara, H. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00458.2005 · Cited by 377 · see citing works
Hierarchical Prediction Errors in Midbrain and Basal Forebrain during Sensory Learning
Iglesias, S., Mathys, C., Brodersen, K. H., Kasper, L., Piccirelli, M., den Ouden, H. E. M., & Stephan, K. E. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.009 · Cited by 342 · 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
“…prior to a block of trials, prior to an individual trial, or contingent on the target, the beneficial influence of reward in all these studies can be readily explained in terms of ongoing top-down attentional control processes (Maunsell, 2004; Stănişor, van der Togt, Pennartz, & Roelfsema, 2013).”
BackgroundRewards teach visual selective attention
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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
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Dissociating valuation and saliency signals during decision-making
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Porter, J. N., Olsen, A. S., Gurnsey, K., Dugan, B. P., Jedema, H. P., & Bradberry, C. W. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5426-10.2011 · Cited by 97 · see citing works
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Watanabe, N., Sakagami, M., & Haruno, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3400-12.2013 · Cited by 65 · see citing works
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Vaidya, A. R., & Fellows, L. K. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1607-15.2015 · Cited by 37 · see citing works
“Attentional bias to reward-associated stimuli is thought to reflect the activation of the behavioral approach system (Gray, 1991; Ikemoto and Panksepp, 1999) or a change in the incentive salience of previously neutral stimuli (Robinson and Berridge, 1993; Maunsell, 2004).”
Background
- Authors
- Maunsell, J. H. R.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Maunsell, John H.R.
- ORCID
- Maunsell, John H.R.
- Venue
- Trends in Cognitive Sciences
- Publisher
- Elsevier BV
- Published
- 2004-06
- Volume
- 8
- Issue
- 6
- Pages
- 261-265
- ISSN
- 1364-6613 (ISSN-L)
- OpenAlex
- W2126116397
- Cited by
- 404
- References
- 39
- Citations by year
- 2026: 13 · 2025: 11 · 2024: 12 · 2023: 6 · 2022: 12 · 2021: 25 · 2020: 17 · 2019: 13 · 2018: 26 · 2017: 20 · 2016: 21 · 2015: 29 · 2014: 32 · 2013: 21 · 2012: 27
- FWCI
- 0.87
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in Cognitive Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Eye Institute (R01EY005911)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- attention, reward anticipation, cognitive states, neural representations, spatial attention, reward contingency, confounding variables
- MeSH terms
- Animals, Attention, Brain, Cognition, Electrophysiology, Humans, Neurons, Reward
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