Abstract
People need to adapt to situations where they experience sequential benefits (or losses) to ensure survival. This study investigated the neural substrates involved in judgments of sequential benefits and losses. A total of 29 healthy volunteers participated in this study, in which they were asked to participate in a game of purchasing stocks while a magnetic resonance imaging scan was performed. This game had two main types of trials: (1) participants received four sequential financial benefits (or losses), and (2) participants received an equal amount of benefits (or losses) immediately. The results showed greater activation of the orbitofrontal cortex (OFC) when four benefits were received sequentially than when an equal amount of benefits was received immediately. This indicates that the OFC plays a crucial role in the process of mental integration of sequential benefits and interpretation of their valuations. It also showed greater activation of the dorsal striatum when four sequental losses were received than when an equal amount of losses was received immediately. However, it cannot be concluded that activation of the dorsal striatum reflects the differences between sequential and immediate losses, because previous studies have not confirmed this perspective. Therefore, it is necessary to clarify the function of the striatum in processing these losses.
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Notes
It is possible that the response time for the game of luck indicates participants’ satisfaction. We examined the relationship between the response time for the game of luck and satisfaction scores using Pearson’s correlation coefficients. The results were as follows: for the 2-day 2 condition, N = 1296, r = −0.09, p < 0.01, and for the 5-day 5 condition, N = 1,296, r = −0.04, ns. Although the results showed a significant negative, weak correlation for the 2-day 2 condition, a strong correlation was not found between the response time for the game of luck and the participants’ satisfaction scores.
References
Akitsuki, Y., Sugiura, M., Watanabe, J., Yamashita, K., Sassa, Y., Awata, S., & Kawashima, R. (2003). Context-dependent cortical activation in response to financial reward and penalty: An event-related fMRI study. NeuroImage, 19, 1674–1685.
Ariely, D. (1998). Combining experiences over time: The effects of duration, intensity changes and on-papers line measurements on retrospective pain evaluation. Journal of Behavioral Decision Making, 11, 19–45.
Balodis, I. M., & Potenza, M. N. (2015). Anticipatory reward processing in addicted populations: A focus on the monetary incentive delay task. Biological Psychiatry, 77, 434–444. https://doi.org/10.1016/j.biopsych.2014.08.020
Balodis, I. M., Kober, H., Worhunsky, P. D., Stevens, M. C., Pearlson, G. D., & Potenza, M. N. (2012). Diminished frontostriatal activity during processing of monetary rewards and losses in pathological gambling. Biological Psychiatry, 71, 749–757. https://doi.org/10.1016/j.biopsych.2012.01.006
Bartra, O., McGuire, J. T., & Kable, J. W. (2013). The valuation system: A coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. NeuroImage, 76, 412–427. https://doi.org/10.1016/j.neuroimage.2013.02.063
Bechara, A., & Damasio, A. (2005). The somatic marker hypothesis: A neural theory of economic decision. Games and Economic Behavior, 52, 336–372.
Bray, S., Shimojo, S., & O'Doherty, J. P. (2010). Human medial orbitofrontal cortex is recruited during experience of imagined and real rewards. Journal of Neurophysiology, 103, 2506–2512.
Breiter, H. C., Aharon, I., Kahneman, D., Dale, A., & Shizgal, P. (2001). Functional imaging of neural responses to monetary gains and losses. Neuron, 30, 619–639.
Christopoulos, G. I., Tobler, P. N., Bossaerts, P., Dolan, R. J., & Schultz, W. (2009). Neural correlates of value, risk, and risk aversion contributing to decision making under risk. Journal of Neuroscience, 29, 12574–12583.
Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., & Zilles, K. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage, 25, 1325–1335.
Eickhoff, S. B., Heim, S., Zilles, K., & Amunts, K. (2006). Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. NeuroImage, 32, 570–582.
Eickhoff, S. B., Paus, T., Caspers, S., Grosbras, M.-H., Evans, A. C., Zilles, K., & Amunts, K. (2007). Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. NeuroImage, 36, 511–521.
Elliott, R., Friston, K. J., & Dolan, R. J. (2000). Dissociable neural responses in human reward systems. Journal of Neuroscience, 20, 6159–6165.
Elliott, R., Agnew, Z., & Deakin, J. F. W. (2008). Medial orbitofrontal cortex codes relative rather than absolute value of financial rewards in humans. European Journal of Neuroscience, 27, 2213–2218.
Feinberg, D. A., Moeller, S., Smith, S. M., Auerbach, E., Ramanna, S., Glasser, M. F., & Yacoub, E. (2010). Multiplexed echo planar imaging for sub-second whole brain fMRI and fast diffusion imaging. PLoS One, 5, e15710.
Filbey, F. M., Dunlop, J., & Myers, U. S. (2013). Neural effects of positive and negative incentives during marijuana withdrawal. PLoS One, 8, e61470. https://doi.org/10.1371/journal.pone.0061470
Flandin, G., & Friston, K. J. (2019). Analysis of family-wise error rates in statistical parametric mapping using random field theory. Human Brain Mapping, 40, 2052–2054.
Friston, K. J., Holmes, A., Poline, J. -B., Price, C. J., & Frith, C. D. (1996). Detecting activations in pet and fMRI: Levels of inference and power. NeuroImage, 4, 223–235.
Friston, K. J., Holmes, A. P., & Worsley, K. J. (1999). How many subjects constitute a study? NeuroImage, 10, 1–5.
Haber, S. N., & Knutson, B. (2010). The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology, 35, 4–26.
Hardin, M. G., Pine, D. S., & Ernst, M. (2009). The influence of context valence in the neural coding of monetary outcomes. NeuroImage, 48, 249–257. https://doi.org/10.1016/j.neuroimage.2009.06.050
Hsee, C. K., & Abelson, R. P. (1991). The velocity relation: Satisfaction as a function of the first derivative of outcome over time. Journal of Personality and Social Psychology, 60, 341–347.
Kahneman, D., & Tversky, A. (1979). Intuitive prediction: Biases and corrective procedures. Management Science, 12, 313–327.
Knutson, B., Adams, C. M., Fong, G. W., & Hommer, D. (2001). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience, 21, RC159.
Knutson, B., Fong, G. W., Bennett, S. M., Adams, C. M., & Hommer, D. (2003). A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: Characterization with rapid event-related fMRI. NeuroImage, 18, 263–272. https://doi.org/10.1016/S1053-8119(02)00057-5
Kohls, G., Perino, M. T., Taylor, J. M., Madva, E. N., Cayless, S. J., Troiani, V., & Schultz, R. T. (2013). The nucleus accumbens is involved in both the pursuit of social reward and the avoidance of social punishment. Neuropsychologia, 51, 2062–2069. https://doi.org/10.1016/j.neuropsychologia.2013.07.020
Kringelbach, M. L., & Rolls, E. T. (2004). The functional neuroanatomy of the human orbitofrontal cortex: Evidence from neuroimaging and neuropsychology. Progress in Neurobiology, 72, 341–372.
Lane, R. D., Reiman, E. M., Ahern, G. L., & Schwartz, G. E. (1997). Neuroanatomical correlates of happiness, sadness, and disgust. The American Journal of Psychiatry, 154, 926–933. https://doi.org/10.1176/ajp.154.7.926
Litt, A., Plassmann, H., Shiv, B., & Rangel, A. (2011). Dissociating valuation and saliency signals during decision-making. Cerebral Cortex, 21, 95–102.
Loewenstein, G., & Prelec, D. (1993). Preferences for sequences of outcomes. Psychological Review, 100, 91–108.
Loewenstein, G., & Sicherman, N. (1991). Do workers prefer increasing wage profile? Journal of Labor Economics, 9, 67–84.
Louie, K., & Glimcher, P. W. (2012). Efficient coding and the neural representation of value. Annals of the New York Academy of Sciences, 1251, 13–32.
Louie, K., Grattan, L. E., & Glimcher, P. W. (2011). Reward value-based gain control: Divisive normalization in parietal cortex. Journal of Neuroscience, 31, 10627–10639.
Moeller, S., Yacoub, E., Olman, C. A., Auerbach, E., Strupp, J., Harel, N., & Uğurbil, K. (2010). Multiband multislice GE-EPI at 7 tesla, with 16-fold acceleration using partial parallel imaging with application to high spatial and temporal whole-brain FMRI. Magnetic Resonance in Medicine, 63, 1144–1153.
Montague, P. R., Dayan, P., & Sejnowski, T. J. (1996). A framework for mesencephalic dopamine systems based on predictive Hebbian learning. Journal of Neuroscience, 16, 1936–1947.
Mullett, T. L., & Tunney, R. J. (2013). Value representations by rank order in a distributed network of varying context dependency. Brain and Cognition, 82, 76–83.
Nelson, L. D., & Meyvis, T. (2008). Interrupted consumption: Disrupting adaptation to hedonic experiences. Journal of Marketing Research, 45, 654–664.
Nelson, L. D., Meyvis, T., & Galak, J. (2009). Enhancing the television-viewing experience through commercial interruptions. Journal of Consumer Research, 36, 160–172. https://doi.org/10.1086/597030
Oldham, S., Murawski, C., Fornito, A., Youssef, G., Yucel, M., & Lorenzetti, V. (2018). The anticipation and outcome phases of reward and loss processing: A neuroimaging meta-analysis of the monetary incentive delay task. Human Brain Mapping, 39, 3398–3418.
Peters, J., & Büchel, C. (2010). Neural representations of subjective reward value. Behavioral Brain Research, 213, 135–141.
Reiman, E. M., Lane, R. D., Ahern, G. L., & Schwartz, G. E. (1997). Neuroanatomical correlates of externally and internally generated human emotion. The American Journal of Psychiatry, 154, 918–925. https://doi.org/10.1176/ajp.154.7.918
Rudorf, S., & Hare, T. A. (2014). Interactions between dorsolateral and ventromedial prefrontal cortex underlie context-dependent stimulus valuation in goal-directed choice. Journal of Neuroscience, 34, 15988–15996.
Sescousse, G., Caldu, X., Segura, B., & Dreher, J. C. (2013). Processing of primary and secondary rewards: A quantitative meta-analysis and review of human functional neuroimaging studies. Neuroscience and Biobehavioral Reviews, 37, 681–696. https://doi.org/10.1016/j.neubiorev.2013.02.002
Seubert, J., Freiher, J., Djordjevic, J., & Lundström, J. N. (2013). Statistical localization of human olfactory cortex. NeuroImage, 66, 333–342.
Skinner, B. F. (1937). Two types of conditioned reflex: A reply to Konorski and Miller. Journal of General Psychology, 16, 272–279.
Skinner, B. F. (1938). The behavior of organisms. Appleton-Century-Crofts.
Staddon, J. E. R., & Cerutti, D. T. (2003). Operant conditioning. Annual Review of Psychology, 54, 115–144.
Tom, S. M., Fox, C. R., Trepel, C., & Poldrack, R. A. (2007). The neural basis of loss aversion in decision-making under risk. Science, 315, 515–518. https://doi.org/10.1126/science.1134239
Tversky, A., & Kahneman, D. (1992). Advances in prospect theory: Cumulative representation of uncertainty. Journal of Risk and Uncertainty, 5, 297–323.
Vermeer, A. B. L., Boksem, M. A. S., & Sanfey, A. G. (2014). Neural mechanisms underlying context-dependent shifts in risk preferences. NeuroImage, 103, 355–363. https://doi.org/10.1016/j.neuroimage.2014.09.054
Vlaev, I., Chater, N., Stewart, N., & Brown, G. D. A. (2011). Does the brain calculate value? Trends in Cognitive Sciences, 15, 546–554.
Xu, J., Moeller, S., Auerbach, E. J., Struppe, J., Smith, S. M., Feinberg, D. A., Yacoub, E., & Uğurbil, K. (2013). Evaluation of slice accelerations using multiband echo planar imaging at 3T. NeuroImage, 83, 991–1001.
Author note
This work was supported by Grant-in-Aid for Scientific Research C 18K03020 from the Japan Society for the Promotion of Science. We thank Prof. Hirohisa Watanabe for his help and support throughout the experiment.
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This work was supported by Grant-in-Aid for Scientific Research C 18K03020 from the Japan Society for the Promotion of Science.
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Noda, M., Tanabe, H.C., Yoshioka, A. et al. Neural substrates on the judgment of sequential benefits and losses. Cogn Affect Behav Neurosci 23, 997–1013 (2023). https://doi.org/10.3758/s13415-023-01087-3
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DOI: https://doi.org/10.3758/s13415-023-01087-3