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A unified selection signal for attention and reward in primary visual cortex
Open accessAbstract
Stimuli associated with high rewards evoke stronger neuronal activity than stimuli associated with lower rewards in many brain regions. It is not well understood how these reward effects influence activity in sensory cortices that represent low-level stimulus features. Here, we investigated the effects of reward information in the primary visual cortex (area V1) of monkeys. We found that the reward value of a stimulus relative to the value of other stimuli is a good predictor of V1 activity. Relative value biases the competition between stimuli, just as has been shown for selective attention. The neuronal latency of this reward value effect in V1 was similar to the latency of attentional influences. Moreover, V1 neurons with a strong value effect also exhibited a strong attention effect, which implies that relative value and top-down attention engage overlapping, if not identical, neuronal selection mechanisms. Our findings demonstrate that the effects of reward value reach down to the earliest sensory processing levels of the cerebral cortex and imply that theories about the effects of reward coding and top-down attention on visual representations should be unified.
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“The “attention-gated reinforcement learning” (AGREL) networks of Stanisor et al. (2013), Brosch et al. (2015), and Roelfsema and van Ooyen (2005), and variants like KickBack (Balduzzi, 2014), give a way to compute an approximation to the full gradient in a reinforcement learning context using a feedback-based attention mechanism for credit assignment within the multi-layer network.”
From Toward an integration of deep learning and neuroscience (2016) · cites this paper as Stanisor et al., 2013
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Citations
Cites
Neural Mechanisms of Selective Visual Attention
Desimone, R., & Duncan, J. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.001205 · Cited by 8,388
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
A framework for studying the neurobiology of value-based decision making
Rangel, A., Camerer, C., & Montague, P. R. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2357 · Cited by 2,184
Neural correlates of decision variables in parietal cortex
Platt, M. L., & Glimcher, P. W. (1999) · Nature · doi:10.1038/22268 · Cited by 1,721
Neurons in the orbitofrontal cortex encode economic value
Padoa-Schioppa, C., & Assad, J. A. (2006) · Nature · doi:10.1038/nature04676 · Cited by 1,598
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
Neuronal Coding of Prediction Errors
Schultz, W., & Dickinson, A. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.473 · Cited by 1,427
Multiple dopamine functions at different time courses
Schultz, W. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135722 · Cited by 1,415
Relative reward preference in primate orbitofrontal cortex
Tremblay, L., & Schultz, W. (1999) · Nature · doi:10.1038/19525 · Cited by 1,314
Matching Behavior and the Representation of Value in the Parietal Cortex
Sugrue, L. P., Corrado, G. S., & Newsome, W. T. (2004) · Science · doi:10.1126/science.1094765 · Cited by 1,030
Attentional modulation of visual motion processing in cortical areas MT and MST
Treue, S., & Maunsell, J. H. R. (1996) · Nature · doi:10.1038/382539a0 · Cited by 1,025
The primate amygdala represents the positive and negative value of visual stimuli during learning
Paton, J. J., Belova, M. A., Morrison, S. E., & Salzman, C. D. (2006) · Nature · doi:10.1038/nature04490 · Cited by 917 · cited 5×
“The computation of relative value requires a comparison between stimuli that can be far apart in the visual field and it is therefore likely that the modulation of V1 activity depends on feedback from higher visual and frontal areas and the amygdala where the representation of reward value depends less on the spatial…”
BackgroundMethodInfluentialThe orbitofrontal cortex: Neuronal activity in the behaving monkey
Thorpe, S. J., Rolls, E. T., & Maddison, S. (1983) · Experimental Brain Research · doi:10.1007/bf00235545 · Cited by 836
Object-based attention in the primary visual cortex of the macaque monkey
Roelfsema, P. R., Lamme, V. A. F., & Spekreijse, H. (1998) · Nature · doi:10.1038/26475 · Cited by 814
Self-citationReward expectancy in primate prefrental neurons
Watanabe, M. (1996) · Nature · doi:10.1038/382629a0 · Cited by 684
Reward Timing in the Primary Visual Cortex
Shuler, M. G. H., & Bear, M. F. (2006) · Science · doi:10.1126/science.1123513 · Cited by 656
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 643
Neuronal Activity Related to Reward Value and Motivation in Primate Frontal Cortex
Roesch, M. R., & Olson, C. R. (2004) · Science · doi:10.1126/science.1093223 · Cited by 535
NEURAL SELECTION AND CONTROL OF VISUALLY GUIDED EYE MOVEMENTS
Schall, J. D., & Thompson, K. G. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.241 · Cited by 489
Leon, M. I., & Shadlen, M. N. (1999) · Neuron · doi:10.1016/s0896-6273(00)80854-5 · Cited by 449
Dorris, M. C., & Glimcher, P. W. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.009 · Cited by 440
CORTICAL ALGORITHMS FOR PERCEPTUAL GROUPING
Roelfsema, P. R. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112939 · Cited by 437
Self-citationModulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study
Armony, J. L. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(01)00178-6 · Cited by 433
Value Representations in the Primate Striatum during Matching Behavior
Lau, B., & Glimcher, P. W. (2008) · Neuron · doi:10.1016/j.neuron.2008.02.021 · Cited by 419
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
Neuronal representations of cognitive state: reward or attention?
Maunsell, J. H. R. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.04.003 · Cited by 404
Neuronal correlates of goal-based motor selection in the prefrontal cortex.
Matsumoto, K., Suzuki, W., & Tanaka, K. (2003) · Science · doi:10.1126/science.1084204 · Cited by 384
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
Value-Based Modulations in Human Visual Cortex
Serences, J. T. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.051 · Cited by 368
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
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 · cited 4×
“Comparable effects have previously been observed in the lateral intraparietal area (area LIP) (21, 24, 36, 41) and in premotor cortex (42), where the relative value of a stimulus has a strong effect but overall reward expectancy does not.”
BackgroundResultInfluentialT HE N EUROBIOLOGY OF V ISUAL -S ACCADIC D ECISION M AKING
Glimcher, P. W. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.010302.081134 · Cited by 297
Modulation of saccadic eye movements by predicted reward outcome
Takikawa, Y., Kawagoe, R., Itoh, H., Nakahara, H., & Hikosaka, O. (2002) · Experimental Brain Research · doi:10.1007/s00221-001-0928-1 · Cited by 287
Dopamine Neurons Can Represent Context-Dependent Prediction Error
Nakahara, H., Itoh, H., Kawagoe, R., Takikawa, Y., & Hikosaka, O. (2004) · Neuron · doi:10.1016/s0896-6273(03)00869-9 · Cited by 276
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
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
The convergence of information about rewarding and aversive stimuli in single neurons
Morrison, S. E., & Salzman, C. D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1815-09.2009 · Cited by 206
Neural Correlates of Biased Competition in Premotor Cortex
Pastor‐Bernier, A., & Cisek, P. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5681-10.2011 · Cited by 181
Preferential Reactivation of Motivationally Relevant Information in the Ventral Striatum
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., Joosten, R. N. J. M. A., McNaughton, B. L., & Pennartz, C. M. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1054-08.2008 · Cited by 168
Self-citationThe Influence of Expected Value on Saccadic Preparation
Milstein, D. M., & Dorris, M. C. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0577-07.2007 · Cited by 144
In Monkeys Making Value-Based Decisions, LIP Neurons Encode Cue Salience and Not Action Value
Leathers, M. L., & Olson, C. R. (2012) · Science · doi:10.1126/science.1226405 · Cited by 133
Attention alters spatial integration in macaque V1 in an eccentricity-dependent manner
Roberts, M. J., Delicato, L. S., Herrero, J. L., Gieselmann, M. A., & Thiele, A. (2007) · Nature Neuroscience · doi:10.1038/nn1967 · Cited by 131
Influences of Rewarding and Aversive Outcomes on Activity in Macaque Lateral Prefrontal Cortex
Kobayashi, S., Nomoto, K., Watanabe, M., Hikosaka, O., Schultz, W., & Sakagami, M. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.031 · Cited by 113
Population Response Profiles in Early Visual Cortex Are Biased in Favor of More Valuable Stimuli
Serences, J. T., & Saproo, S. (2010) · Journal of Neurophysiology · doi:10.1152/jn.01090.2009 · Cited by 100
Neuronal Activity Related to Anticipated Reward in Frontal Cortex
Roesch, M. R., & Olson, C. R. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1401.004 · Cited by 93
Subtask sequencing in the primary visual cortex
Roelfsema, P. R., Khayat, P. S., & Spekreijse, H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0431051100 · Cited by 84
Self-citationvan Duuren, E., Plasse, G., Lankelma, J. V., Joosten, R. N. J. M. A., Feenstra, M. G. P., & Pennartz, C. M. A. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0005-09.2009 · Cited by 80
Self-citationHoutkamp, R., Spekreijse, H., & Roelfsema, P. R. (2003) · Perception & Psychophysics · doi:10.3758/bf03194840 · Cited by 73
Self-citationNoise Correlations Have Little Influence on the Coding of Selective Attention in Area V1
Poort, J., & Roelfsema, P. R. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn103 · Cited by 59
Self-citation
Research works printed but not linked: 1
- National Research Council Committee for the Update of the Guide for the Care and Use of Laboratory Animals and Institute for Laboratory Animal Research (2011) Guide for the Care and Use of Laboratory Animals (National Academies Press Washington DC) 8th Ed.
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Neuronal Reward and Decision Signals: From Theories to Data
Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126
Dopamine reward prediction-error signalling: A two-component response
Schultz, W. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.26 · Cited by 1,036
Learning Enhances Sensory and Multiple Non-sensory Representations in Primary Visual Cortex
Poort, J., Khan, A. G., Pachitariu, M., Nemri, A., Oršolić, I., Krupic, J., Bauža, M., Sahani, M., Keller, G. B., Mrsic‐Flogel, T. D., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.037 · Cited by 405
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
Neuronal Mechanisms of Visual Attention
Maunsell, J. H. R. (2015) · Annual Review of Vision Science · doi:10.1146/annurev-vision-082114-035431 · Cited by 346
Metadata
- Authors
- Stănişor, L., van der Togt, C., Pennartz, C. M. A., & Roelfsema, P. R.
- Affiliations
- Netherlands Institute for Neuroscience (NL)
- Department of Vision and Cognition, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, 1105 BA Amsterdam, The Netherlands;
- University of Amsterdam (NL)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-05-15
- Volume
- 110
- Issue
- 22
- Pages
- 9136-9141
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3670348
- OpenAlex
- W2128585328
- Cited by
- 158
- References
- 49
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 10 · 2023: 10 · 2022: 13 · 2021: 10 · 2020: 15 · 2019: 11 · 2018: 16 · 2017: 12 · 2016: 15 · 2015: 22 · 2014: 12 · 2013: 1
- FWCI
- 9.11
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- VU Research Portal (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Visual Attention and Saliency Detection
- Keywords
- primary visual cortex, reward value, top-down attention, relative value, stimulus competition, attentional modulation, reward coding, visual representation, neuronal latency, monkeys
- MeSH terms
- Action Potentials, Analysis of Variance, Animals, Haplorhini, Attention, Color, Cues, Psychomotor Performance, Reaction Time, Reward, Saccades, Visual Cortex
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