Abstract
Normatively, our decisions ought to be made relative to our total wealth, but in practice, we make our decisions relative to variable, decision-time-specific set points. This predilection introduces a major behavioral bias that is known as reference-point dependence in Prospect Theory, and it has close links to mental accounting. Here we examined neural activity in the dorsal anterior cingulate cortex (dACC) of macaques performing a token-based risky choice task, in which the acquisition of six tokens (accumulated over several trials) resulted in a jackpot reward. We found that subjects make faster and more accurate choices, and that they are less prone to risk-taking as offer contingencies are easier and the jackpot reward becomes more likely to be achieved. By comparing alternative models that accounted for progressive token accumulation, we found that subjective evaluations are best explained by a reference-dependent value ‘RDV’ model where offer values are considered as potential gains or losses with respect to a token-dependent reference. The reference-dependent model allows to implement a dynamical comparison of the two offered values to each other and to the number of missing tokens to reach the six-tokens threshold as jackpot approaches. In dACC, we find that gains in subjective values entail higher fractions of encoding cells than losses, and that the encoding tuning of expected utility variables is best aligned with upcoming choices in gains than in losses. These results suggest a neural basis of reference dependence biases in shaping decision-making behavior and highlight the critical role of value representations in dACC in driving evaluations.
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Data availability
Data used in this study is available at the https://doi.org/10.12751/g-node.1kkrw6.
Code availability
Code developed for the presented analyses is available at the https://doi.org/10.12751/g-node.1kkrw6.
References
Kahneman, D. & Tversky, A. Prospect Theory: An Analysis of Decision under Risk. Econ. Soc. 47, 263–291 (1979).
Anke Braun, X., Urai, A. E., Tobias, X. & Donner, H. Adaptive history biases result from confidence-weighted accumulation of past choices. J. Neurosci. 38, 2418-2429 (2018).
Nogueira, R. et al. Lateral orbitofrontal cortex anticipates choices and integrates prior with current information. Nat Commun 8, 14823 (2017).
Mochol, G., Kiani, R. & Moreno-Bote, R. Prefrontal cortex represents heuristics that shape choice bias and its integration into future behavior. Curr. Biol. 31, 1234–1244.e6 (2021).
Hermoso-Mendizabal, A. et al. Response outcomes gate the impact of expectations on perceptual decisions. Nat Commun 11, 1057 (2020).
Padoa-Schioppa, C. & Assad, J. A. Neurons in the orbitofrontal cortex encode economic value. Nature 441, 223–226 (2006).
Bartra, O., McGuire, J. T. & Kable, J. W. The valuation system: a coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. Neuroimage 76, 412–427 (2013).
Ebitz, R. B. & Hayden, B. Y. Dorsal anterior cingulate: a Rorschach test for cognitive neuroscience. Nat. Neurosci. 19, 1278–1279 (2016).
Haber, S. N. & Behrens, T. E. J. The neural network underlying incentive-based learning: implications for interpreting circuit disruptions in psychiatric disorders. Neuron 83, 1019–1039 (2014).
Heilbronner, S. R. & Hayden, B. Y. Dorsal anterior cingulate cortex: a bottom-up view. Annu. Rev. Neurosci. 39, 149–170 (2016).
Kable, J. W. & Glimcher, P. W. The neural correlates of subjective value during intertemporal choice. Nat. Neurosci. 10, 1625–1633 (2007).
Camille, N., Griffiths, C. A., Vo, K., Fellows, L. K. & Kable, J. W. Ventromedial frontal lobe damage disrupts value maximization in humans. J. Neurosci. 31, 7527–7532 (2011).
Rushworth, M. F. S. & Behrens, T. E. J. Choice, uncertainty and value in prefrontal and cingulate cortex. Nat. Neurosci. 11, 389–397 (2008).
Rushworth, M. F. S., Noonan, M. A. P., Boorman, E. D., Walton, M. E. & Behrens, T. E. Frontal cortex and reward-guided learning and decision-making. Neuron 70, 1054–1069 (2011).
Kennerley, S. W., Behrens, T. E. J. & Wallis, J. D. Double dissociation of value computations in orbitofrontal and anterior cingulate neurons. Nat. Neurosci. 14, 1581–1589 (2011).
Wallis, J. D. Orbitofrontal cortex and its contribution to decision-making. Annu. Rev. Neurosci. 30, 31–56 (2007).
Rich, E. L. & Wallis, J. D. Decoding subjective decisions from orbitofrontal cortex. Nat. Neurosci. 19, 973–980 (2016).
Padoa-Schioppa, C. Neuronal origins of choice variability in economic decisions. Neuron 80, 1322–1336 (2013).
Strait, C. E., Blanchard, T. C. & Hayden, B. Y. Reward value comparison via mutual inhibition in ventromedial prefrontal cortex. Neuron 82, 1357–1366 (2014).
Ferro, D., Cash-Padgett, T., Wang, M. Z., Hayden, B. Y. & Moreno-Bote, R. Gaze-centered gating, reactivation, and reevaluation of economic value in orbitofrontal cortex. Nat. Commun 15, (2024).
Maisson, D. J. N. et al. Choice-relevant information transformation along a ventrodorsal axis in the medial prefrontal cortex. Nat. Commun. 12, 4830 (2021).
Juechems, K., Balaguer, J., Ruz, M. & Summerfield, C. Ventromedial prefrontal cortex encodes a latent estimate of cumulative reward. Neuron 93, 705–714.e4 (2017).
Botvinick, M., Nystrom, L. E., Fissell, K., Carter, C. S. & Cohen, J. D. Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402, 179–181 (1999).
Van Veen, V., Cohen, J. D., Botvinick, M. M., Stenger, V. A. & Carter, C. S. Anterior cingulate cortex, conflict monitoring, and levels of processing. Neuroimage 14, 1302–1308 (2001).
Botvinick, M. M., Cohen, J. D. & Carter, C. S. Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn. Sci. 8, 539–546 (2004).
Shenhav, A., Botvinick, M. M. & Cohen, J. D. The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron 79, 217–240 (2013).
Hadland, K. A., Rushworth, M. F. S., Gaffan, D. & Passingham, R. E. The anterior cingulate and reward-guided selection of actions. J. Neurophysiol. 89, 1161–1164 (2003).
Vassena, E., Holroyd, C. B. & Alexander, W. H. Computational models of anterior cingulate cortex: At the crossroads between prediction and effort. Front. Neurosci. 11, (2017).
Vassena, E., Deraeve, J. & Alexander, W. H. Surprise, value and control in anterior cingulate cortex during speeded decision-making. Nat. Hum. Behav. 4, 412–422 (2020).
Vassena, E. et al. Overlapping neural systems represent cognitive effort and reward anticipation. PLoS One 9, (2014).
Kurniawan, I. T., Guitart-Masip, M., Dayan, P. & Dolan, R. J. Effort and valuation in the brain: The effects of anticipation and execution. J. Neurosci. 33, 6160–6169 (2013).
Goh, A. X. A., Bennett, D., Bode, S. & Chong, T. T. J. Neurocomputational mechanisms underlying the subjective value of information. Commun. Biol. 4, (2021).
Amiez, C., Joseph, J. P. & Procyk, E. Anterior cingulate error-related activity is modulated by predicted reward. Eur. J. Neurosci. 21, 3447–3452 (2005).
Blanchard, T. C., Strait, C. E. & Hayden, B. Y. Ramping ensemble activity in dorsal anterior cingulate neurons during persistent commitment to a decision. J. Neurophysiol. 114, 2439–2449 (2015).
Bush, G. et al. Dorsal Anterior Cingulate Cortex: A Role in Reward-Based Decision Making, Vol. 99, https://doi.org/10.1073/pnas.012470999 (2002).
Aarts, E. & Roelofs, A. Attentional Control in Anterior Cingulate Cortex Based on Probabilistic Cueing. J. Cogn. Neurosci. 23, 716–727 (2011).
Strait, C. E. et al. Neuronal selectivity for spatial positions of offers and choices in five reward regions. J. Neurophysiol. 115, 1098–1111 (2016).
Azab, H. & Hayden, B. Y. Correlates of decisional dynamics in the dorsal anterior cingulate cortex. PLoS Biol. 15, (2017).
Azab, H. & Hayden, B. Y. Correlates of economic decisions in the dorsal and subgenual anterior cingulate cortices. Eur. J. Neurosci. 47, 979–993 (2018).
Farashahi, S., Azab, H., Hayden, B. & Soltani, A. On the flexibility of basic risk attitudes in monkeys. J. Neurosci. 38, 4383–4398 (2018).
Blanchard, T. C. & Hayden, B. Y. Neurons in dorsal anterior cingulate cortex signal postdecisional variables in a foraging task. J. Neurosci. 34, 646–655 (2014).
Shidara, M. & Richmond, B. J. Anterior Cingulate: Single Neuronal Signals Related to Degree of Reward Expectancy. Science 296, 1709–1711 (2002).
Cai, X. & Padoa-Schioppa, C. Neuronal activity in dorsal anterior cingulate cortex during economic choices under variable action costs. Elife 10, (2021).
Hayden, B. Y., Pearson, J. M. & Platt, M. L. Fictive reward signals in the anterior cingulate cortex. Science 324, 948–950 (2009). 1979.
Kerns, J. G. et al. Anterior cingulate conflict monitoring and adjustments in control. Science 303, 1023–1026 (2004).
Hayden, B. Y., Heilbronner, S. R., Pearson, J. M. & Platt, M. L. Surprise signals in anterior cingulate cortex: Neuronal encoding of unsigned reward prediction errors driving adjustment in behavior. J. Neurosci. 31, 4178–4187 (2011).
Bos, W. V. anD. en & McClure, S. M. Towards a general model of temporal discounting. J. Exp. Anal. Behav. 99, 58–73 (2013).
Kim, S., Hwang, J. & Lee, D. Prefrontal coding of temporally discounted values during intertemporal choice. Neuron 59, 161–172 (2008).
Louie, K. & Glimcher, P. W. Separating value from choice: delay discounting activity in the lateral intraparietal area. J. Neurosci. 30, 5498–5507 (2010).
Blanchard, T. C., Pearson, J. M. & Hayden, B. Y. Postreward delays and systematic biases in measures of animal temporal discounting. Proc. Natl. Acad. Sci. USA 110, 15491–15496 (2013).
Hayden, B. Y. Time discounting and time preference in animals: a critical review. Psychon. Bull. Rev. 23, 39–53 (2016).
Tversky, A. & Kahneman, D. Judgment under uncertainty: heuristics and biases in judgments reveal some heuristics of thinking under uncertainty. Science 185, 1124–1131 (1974).
Tversky, A. & Kahneman, D. Advances in prospect theory: cumulative representation of uncertainty. J. Risk Uncertain. 5, 297–323 (1992).
O’Doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J. & Andrews, C. Abstract reward and punishment representations in the human orbitofrontal cortex. Nat. Neurosci. 4, 95–102 (2001).
Tobler, P. N., O’Doherty, J. P., Dolan, R. J. & Schultz, W. Reward value coding distinct from risk attitude-related uncertainty coding in human reward systems. J. Neurophysiol. 97, 1621–1632 (2007).
Lee, D., Seo, H. & Jung, M. W. Neural basis of reinforcement learning and decision making. Annu. Rev. Neurosci. 35, 287–308 (2012).
Holroyd, C. B. & Yeung, N. Motivation of extended behaviors by anterior cingulate cortex. Trends Cogn. Sci. 16, 122–128 (2012).
Sallet, J. et al. Expectations, gains, and losses in the anterior cingulate cortex. Cogn. Affect Behav. Neurosci. 7, 327–336 (2007).
Hajnal, M. A. et al. Shifts in attention drive context-dependent subspace encoding in anterior cingulate cortex in mice during decision making. Nat. Commun. 15, (2024).
Weissman, D. H., Gopalakrishnan, A., Hazlett, C. J. & Woldorff, M. G. Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. Cereb. Cortex 15, 229–237 (2005).
Lake, J. I. et al. Reward anticipation and punishment anticipation are instantiated in the brain via opponent mechanisms. Psychophysiology 56, (2019).
Aarts, E., Roelofs, A. & Van Turennout, M. Anticipatory activity in anterior cingulate cortex can be independent of conflict and error likelihood. J. Neurosci. 28, 4671–4678 (2008).
Meder, D., Herz, D. M., Rowe, J. B., Lehéricy, S. & Siebner, H. R. The role of dopamine in the brain - lessons learned from Parkinson’s disease. NeuroImage 190, 79–93 (2019).
Berridge, K. C. & Robinson, T. E. Parsing reward. Trends Neurosci. 26, 507–513 (2003).
Glimcher, P. W. Understanding dopamine and reinforcement learning: The dopamine reward prediction error hypothesis. Proc. Natl. Acad. Sci. USA 108, 15647–15654 (2011).
Westbrook, A. et al. Dopamine promotes cognitive effort by biasing the benefits versus costs of cognitive work. Science 367, 1362–1366 (2020).
Chakroun, K. et al. Dopamine regulates decision thresholds in human reinforcement learning in males. Nat. Commun. 14, (2023).
Kennerley, S. W., Walton, M. E., Behrens, T. E. J., Buckley, M. J. & Rushworth, M. F. S. Optimal decision making and the anterior cingulate cortex. Nat. Neurosci. 9, 940–947 (2006).
Morcos, A. S. & Harvey, C. D. History-dependent variability in population dynamics during evidence accumulation in cortex. Nat. Neurosci. 19, 1672–1681 (2016).
Abrahamyan, A., Silva, L. L., Dakin, S. C., Carandini, M. & Gardner, J. L. Adaptable history biases in human perceptual decisions. Proc. Natl. Acad. Sci. USA 113, E3548–E3557 (2016).
McGinty, V. B. & Lupkin, S. M. Behavioral read-out from population value signals in primate orbitofrontal cortex. Nat. Neurosci. 26, 2203–2212 (2023).
Acknowledgements
This project was supported by grants funded by the Spanish Ministry of Science, Innovation and Universities (MICIU/AEI/10.13039/501100011033) and by “FEDER A way of making Europe” (ref: PID2023-146524NB), and by ICREA ACADÈMIA (2022) funded by the Catalan Institution for Research and Advanced Studies to R.M.B.
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D.F., R.M.B. conceptualized and designed the analyses. B.H. ideated the task. D.F. analyzed the data. B.H., H.A. collected the data. D.F., B.H., R.M.B. wrote the manuscript.
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Ferro, D., Azab, H., Hayden, B.Y. et al. Accumulation of virtual tokens towards a jackpot reward enhances performance and value encoding in dorsal anterior cingulate cortex. Nat Commun (2026). https://doi.org/10.1038/s41467-026-70423-1
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DOI: https://doi.org/10.1038/s41467-026-70423-1
