How the brain integrates costs and benefits during decision making
Open accessAbstract
When we make decisions, the benefits of an option often need to be weighed against accompanying costs. Little is known, however, about the neural systems underlying such cost–benefit computations. Using functional magnetic resonance imaging and choice modeling, we show that decision making based on cost–benefit comparison can be explained as a stochastic accumulation of cost–benefit difference. Model-driven functional MRI shows that ventromedial and left dorsolateral prefrontal cortex compare costs and benefits by computing the difference between neural signatures of anticipated benefits and costs from the ventral striatum and amygdala, respectively. Moreover, changes in blood oxygen level dependent (BOLD) signal in the bilateral middle intraparietal sulcus reflect the accumulation of the difference signal from ventromedial prefrontal cortex. In sum, we show that a neurophysiological mechanism previously established for perceptual decision making, that is, the difference-based accumulation of evidence, is fundamental also in value-based decisions. The brain, thus, weighs costs against benefits by combining neural benefit and cost signals into a single, difference-based neural representation of net value, which is accumulated over time until the individual decides to accept or reject an option.
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Prior work has established that the ventromedial prefrontal cortex (vmPFC) plays a central role in computing the value of potential choice options, with activity in this region reflecting the dynamic evolution of a value comparison.
“Prior work has established that the ventromedial prefrontal cortex (vmPFC) plays a central role in computing the value of potential choice options1-5, with activity in this region reflecting the dynamic evolution of a value comparison6.”
From Confidence in value-based choice (2013) · cites this paper as [4]
Cites
Ratcliff, R. (1978) · Psychological Review · doi:10.1037/0033-295x.85.2.59 · Cited by 4,513 · see citing works
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
Bayesian t tests for accepting and rejecting the null hypothesis
Rouder, J. N., Speckman, P. L., Sun, D., Morey, R. D., & Iverson, G. (2009) · Psychonomic Bulletin & Review · doi:10.3758/pbr.16.2.225 · Cited by 3,688 · see citing works
Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910330508 · Cited by 3,202 · see citing works
Psychophysiological and Modulatory Interactions in Neuroimaging
Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., & Dolan, R. J. (1997) · NeuroImage · doi:10.1006/nimg.1997.0291 · Cited by 3,097 · see citing works
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 · see citing works
The time course of perceptual choice: The leaky, competing accumulator model.
Usher, M., & McClelland, J. L. (2001) · Psychological Review · doi:10.1037/0033-295x.108.3.550 · Cited by 2,152 · see citing works
Decision field theory: a dynamic-cognitive approach to decision making in an uncertain environment.
Busemeyer, J., & Townsend, J. (1993) · Psychology Review · doi:10.1037/0033-295x.100.3.432 · Cited by 2,000 · see citing works
Bechara, A., Tranel, D., & Damásio, H. (2000) · Brain · doi:10.1093/brain/123.11.2189 · Cited by 1,919 · see citing works
Dissociation Of Working Memory from Decision Making within the Human Prefrontal Cortex
Bechara, A., Damásio, H., Tranel, D., & Anderson, S. W. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00428.1998 · Cited by 1,059 · see citing works
Psychology and neurobiology of simple decisions
Smith, P. L., & Ratcliff, R. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.01.006 · Cited by 1,051 · see citing works
Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque
Kim, J.-N., & Shadlen, M. N. (1999) · Nature Neuroscience · doi:10.1038/5739 · Cited by 950 · 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
The neural systems that mediate human perceptual decision making
Heekeren, H. R., Marrett, S., & Ungerleider, L. G. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2374 · Cited by 877 · see citing works
Self-citationA 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
Self-citationFunctional magnetic resonance imaging of reward prediction
Knutson, B., & Cooper, J. C. (2005) · Current Opinion in Neurology · doi:10.1097/01.wco.0000173463.24758.f6 · Cited by 736 · see citing works
The effect of stimulus strength on the speed and accuracy of a perceptual decision
Palmer, J., Huk, A. C., & Shadlen, M. N. (2005) · Journal of Vision · doi:10.1167/5.5.1 · Cited by 691 · see citing works
Chib, V. S., Rangel, A., Shimojo, S., & O'Doherty, J. P. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2575-09.2009 · Cited by 643 · see citing works
A role for neural integrators in perceptual decision making
Mazurek, M. E., Roitman, J. D., Ditterich, J., & Shadlen, M. N. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg097 · Cited by 620 · see citing works
Dissociating working memory from task difficulty in human prefrontal cortex
Barch, D. M., Braver, T. S., Nystrom, L. E., Forman, S. D., Noll, D. C., & Cohen, J. D. (1997) · Neuropsychologia · doi:10.1016/s0028-3932(97)00072-9 · Cited by 591 · see citing works
Yacubian, J., Gläscher, J., Schroeder, K., Sommer, T., Braus, D. F., & Büchel, C. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2915-06.2006 · Cited by 537 · see citing works
Model‐Based fMRI and Its Application to Reward Learning and Decision Making
O’Doherty, J. P., Hampton, A. N., & Kim, H. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1390.022 · Cited by 509 · see citing works
Cortico–basal ganglia circuit mechanism for a decision threshold in reaction time tasks
Lo, C.-C., & Wang, X.-J. (2006) · Nature Neuroscience · doi:10.1038/nn1722 · Cited by 505 · see citing works
Paus, T., Koski, L. M., Caramanos, Z., & Westbury, C. F. (1998) · Neuroreport · doi:10.1097/00001756-199806220-00001 · Cited by 462 · see citing works
An automatic valuation system in the human brain: Evidence from functional neuroimaging
Lebreton, M., Jorge, S., Michel, V., Thirion, B., & Pessiglione, M. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.040 · Cited by 455 · see citing works
Amygdala damage eliminates monetary loss aversion
De Martino, B., Camerer, C. F., & Adolphs, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910230107 · Cited by 444 · cited 3× · see citing works
“At the brain level, we hypothesized that the decision process involves separate representations of expected reward and loss, in the ventral striatum (1) and amygdala (14, 15), respectively, from which a comparison signal is computed.”
BackgroundMethodResultPhiliastides, M. G., Ratcliff, R., & Sajda, P. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1655-06.2006 · Cited by 394 · see citing works
Gläscher, J., Hampton, A. N., & O'Doherty, J. P. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn098 · Cited by 387 · see citing works
Fellows, L. K., & Farah, M. J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl176 · Cited by 337 · see citing works
Functional Imaging of Decision Conflict
Pochon, J.-B., Riis, J., Sanfey, A. G., Nystrom, L. E., & Cohen, J. D. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4195-07.2008 · Cited by 179 · see citing works
Fellows, L. K. (2006) · Brain · doi:10.1093/brain/awl017 · Cited by 162 · see citing works
A mechanistic account of value computation in the human brain
Philiastides, M. G., Biele, G., & Heekeren, H. R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1001732107 · Cited by 144 · see citing works
Self-citationThe Functional Anatomy of a Perceptual Decision in the Human Brain
Kayser, A. S., Buchsbaum, B. R., Erickson, D. T., & D’Esposito, M. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00364.2009 · Cited by 118 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Diffusion decision model: Current issues and history
Ratcliff, R., Smith, P. L., Brown, S. D., & McKoon, G. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.01.007 · Cited by 1,630 · see citing works
“Many studies have established relationships between diffusion models and neurophysiological measures such as single cell recordings in rodents and monkeys [52,88,105,143–148], EEG [42,43,149,150], fMRI [42,43,139,151–155], transcranial magnetic stimulation (TMS) [156], and transcranial alternating current stimulation…”
BackgroundThe root of all value: a neural common currency for choice
Levy, D. J., & Glimcher, P. W. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.06.001 · Cited by 1,342 · see citing works
Frontal cortex and reward-guided learning and decision-making
Rushworth, M. F. S., Noonan, M. P., Boorman, E. D., Walton, M. E., & Behrens, T. E. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.014 · Cited by 1,111 · see citing works
Informatic parcellation of the network involved in the computation of subjective value
Clithero, J. A., & Rangel, A. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst106 · Cited by 706 · see citing works
Kolling, N., Behrens, T. E. J., Mars, R. B., & Rushworth, M. F. S. (2012) · Science · doi:10.1126/science.1216930 · Cited by 629 · see citing works
Neurophysiology of performance monitoring and adaptive behavior
Ullsperger, M., Danielmeier, C., & Jocham, G. (2014) · Physiological Reviews · doi:10.1152/physrev.00041.2012 · Cited by 634 · see citing works
Hare, T. A., Malmaud, J., & Rangel, A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6383-10.2011 · Cited by 556 · see citing works
Confidence in value-based choice
De Martino, B., Fleming, S. M., Garrett, N., & Dolan, R. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3279 · Cited by 534 · 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
Lim, S.-L., O'Doherty, J. P., & Rangel, A. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.1246-11.2011 · Cited by 329 · see citing works
Mapping value based planning and extensively trained choice in the human brain
Wunderlich, K., Dayan, P., & Dolan, R. J. (2012) · Nature Neuroscience · doi:10.1038/nn.3068 · Cited by 310 · see citing works
A Neurocomputational Model of Altruistic Choice and Its Implications
Hutcherson, C. A., Bushong, B., & Rangel, A. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.031 · Cited by 299 · see citing works
Valuation and decision-making in frontal cortex: one or many serial or parallel systems?
Rushworth, M. F., Kolling, N., Sallet, J., & Mars, R. B. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.04.011 · Cited by 309 · see citing works
Reward value comparison via mutual inhibition in ventromedial prefrontal cortex
Strait, C. E., Blanchard, T. C., & Hayden, B. Y. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.032 · Cited by 294 · see citing works
Hutcherson, C. A., Plassmann, H., Gross, J. J., & Rangel, A. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.6387-11.2012 · Cited by 227 · 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
Overlapping neural systems represent cognitive effort and reward anticipation
Vassena, E., Silvetti, M., Boehler, C. N., Achten, E., Fias, W., & Verguts, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091008 · Cited by 200 · see citing works
Summerfield, C., & Tsetsos, K. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00070 · Cited by 167 · see citing works
Noonan, M. P., Chau, B. K. H., Rushworth, M. F. S., & Fellows, L. K. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.0692-17.2017 · Cited by 167 · see citing works
Pfeiffer, U. J., Schilbach, L., Timmermans, B., Kuzmanovic, B., Georgescu, A. L., Bente, G., & Vogeley, K. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.06.061 · Cited by 155 · see citing works
Sebastian, A., Jung, P., Krause-Utz, A., Lieb, K., Schmahl, C., & Tüscher, O. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00698 · Cited by 156 · see citing works
“Prefrontal activation and information sampling Information sampling has been shown to rely on ventromedial prefrontal regions and the left DLPFC (Heekeren et al., 2008; Basten et al., 2010).”
BackgroundReasoning supports utilitarian resolutions to moral dilemmas across diverse measures.
Patil, I., Zucchelli, M. M., Kool, W., Campbell, S., Fornasier, F., Calò, M., Silani, G., Cikara, M., & Cushman, F. (2021) · Journal of Personality and Social Psychology · doi:10.1037/pspp0000281 · Cited by 133 · see citing works
Ziegler, S., Pedersen, M. L., Mowinckel, A. M., & Biele, G. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.002 · Cited by 110 · see citing works
Self-citationSelective involvement by the medial orbitofrontal cortex in biasing risky, but not impulsive, choice
Stopper, C. M., Green, E. B., & Floresco, S. B. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhs297 · Cited by 117 · see citing works
Hosking, J. G., Cocker, P. J., & Winstanley, C. A. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.27 · Cited by 119 · see citing works
How Expert Advice Influences Decision Making
Meshi, D., Biele, G., Korn, C. W., & Heekeren, H. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049748 · Cited by 107 · see citing works
Self-citationRats adopt the optimal timescale for evidence integration in a dynamic environment
Piet, A. T., El Hady, A., & Brody, C. D. (2018) · Nature Communications · doi:10.1038/s41467-018-06561-y · Cited by 76 · see citing works
Anterior insula reflects surprise in value-based decision-making and perception
Loued-Khenissi, L., Pfeuffer, A., Einhäuser, W., & Preuschoff, K. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116549 · Cited by 66 · see citing works
Trudel, N., Scholl, J., Klein-Flügge, M. C., Fouragnan, E., Tankelevitch, L., Wittmann, M. K., & Rushworth, M. F. S. (2020) · Nature Human Behaviour · doi:10.1038/s41562-020-0929-3 · Cited by 74 · see citing works
Kroemer, N. B., Guevara, A., Ciocanea Teodorescu, I., Wuttig, F., Kobiella, A., & Smolka, M. N. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.07.060 · Cited by 64 · see citing works
- Authors
- Basten, U., Biele, G., Heekeren, H. R., & Fiebach, C. J.
- Affiliations
- Goethe University Frankfurt (DE)
- Max Planck Society (DE)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-11-30
- Volume
- 107
- Issue
- 50
- Pages
- 21767-21772
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3003102
- OpenAlex
- W2137984543
- Cited by
- 466
- References
- 33
- Citations by year
- 2026: 19 · 2025: 25 · 2024: 22 · 2023: 24 · 2022: 30 · 2021: 35 · 2020: 33 · 2019: 33 · 2018: 23 · 2017: 28 · 2016: 24 · 2015: 39 · 2014: 63 · 2013: 32 · 2012: 23
- FWCI
- 13.36
- 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)
- RePEc: Research Papers in Economics (submittedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- 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
- cost-benefit decision making, value-based decision making, ventromedial prefrontal cortex, dorsolateral prefrontal cortex, ventral striatum, amygdala, choice modeling
- MeSH terms
- Animals, Brain, Choice Behavior, Cost-Benefit Analysis, Decision Making, Humans, Magnetic Resonance Imaging, Male, Oxygen, Psychomotor Performance, Prefrontal Cortex, Young Adult
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