Neural correlates of opponent processes for financial gains and losses

ERDENIZ, BURAK; Done, John

doi:10.5152/NSN.2019.10942

Neural correlates of opponent processes for financial gains and losses

Burak Erdeniz, (Department of Psychology, İzmir University of Economics, Faculty of Arts and Sciences, İzmir, Turkey)

John Done (Department of Psychology and Sports Sciences, School of Life and Medical Sciences, Hatfield, United Kingdom)

Neurological sciences and neurophysiology (Online)

1 0

Yıl: 2019 Cilt: 36 Sayı: 2 Sayfa Aralığı: 69 - 77 Metin Dili: İngilizce DOI: 10.5152/NSN.2019.10942 İndeks Tarihi: 17-08-2020

Neural correlates of opponent processes for financial gains and losses

Öz:

Objective: Functional imaging studies offer alternative explanations for the neural correlates of monetary gain and loss relatedbrain activity, and their opponents, omission of gains and losses. One possible explanation based on the psychology of opponent process theory suggests that successful avoidance of an aversive outcome is itself rewarding, and hence activates brain regions involved in reward processing. In order to test this hypothesis, we compared brain activation for successful avoidance of losses and receipt of monetary gains. Additionally, the brain regions involved in processing of frustrative neutral outcomes and actual losses were compared in order to test whether these two representations are coded in common or distinct brain regions. Methods: Using a 3 Tesla functional magnetic resonance imaging machine, fifteen healthy volunteers between the ages 22 to 28 were scanned for blood oxygen level dependent signal changes while they were performing a probabilistic learning task, wherein each trial a participant chose one of the two available options in order to win or avoid losing money. Results: The results confirmed, previous findings showing that medial frontal cortex and ventral striatum show significant activation (p<0.001) not only for monetary gains but also for successful avoidance of losses. A similar activation pattern was also observed for monetary losses and avoidance of gains in the medial frontal cortex, and posterior cingulate cortex, however, there was increased activation in amygdala specific to monetary losses (p<0.001). Further, subtraction analysis showed that regardless of the type of loss (i.e., frustrative neutral outcomes) posterior insula showed increased activation. Conclusion: This study provides evidence for a significant overlap not only between gains and losses, but also between their opponents. The results suggested that the overlapping activity pattern in the medial frontal cortex could be explained by a more abstract function of medial frontal cortex, such as outcome evaluation or performance monitoring, which possibly does not differentiate between winning and losing monetary outcomes.

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1. Rangel A, Camerer C, Montague PR. A framework for studying the neurobiology of value-based decision making. Nat Rev Neu-rosci 2008; 9: 545-556. [CrossRef]
2. Seymour B, Singer T, Dolan R. The neurobiology of punishment. Nat Rev Neurosci 2007; 8: 300-311. [CrossRef] 3. Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA. Tracking the hemodynamic responses to reward and punishment in the stri-atum. J Neurophysiol 2000; 84: 3072-3077. [CrossRef]
4. Delgado MR, Jou RL, Phelps EA. Neural systems underlying aver-sive conditioning in humans with primary and secondary rein-forcers. Front Neurosci 2011; 5: 71. [CrossRef]
5. Jensen J, McIntosh AR, Crawley AP, Mikulis DJ, Remington G, Ka-pur S. Direct activation of the ventral striatum in anticipation of aversive stimuli. Neuron 2003; 40: 1251-1257. [CrossRef]
6. D'Ardenne K, McClure SM, Nystrom LE, Cohen JD. BOLD re-sponses reflecting dopaminergic signals in the human ventral tegmental area. Science 2008; 319: 1264-1267. [CrossRef]
7. Berns GS, McClure SM, Pagnoni G, Montague PR. Predictability modulates human brain response to reward. J Neurosci 2001; 21: 2793-2798. [CrossRef]
8. O’Doherty JP. Reward representations and reward-related learn-ing in the human brain: insights from neuroimaging. Curr Opin Neurobiol 2004; 14: 769-766. [CrossRef]
9. Camara E, Rodriguez-Fornells A, Münte TF. Functional connec-tivity of reward processing in the brain. Front Hum Neurosci 2009; 2: 19. [CrossRef]
10. Camara E, Rodriguez-Fornells A, Ye Z, Münte TF. Reward net-works in the brain as captured by connectivity measures. Front Neurosci 2009; 3: 350-362. [CrossRef]
11. Dreher JC, Grafman J. Dissociating the roles of the rostral anterior cin-gulate and the lateral prefrontal cortices in performing two tasks simul-taneously or successively. Cereb Cortex 2003; 13: 329-339. [CrossRef]
12. Gottfried JA, O’Doherty J, Dolan RJ. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 2003; 301: 1104-1107. [CrossRef]
13. Nieuwenhuis S, Heslenfeld DJ, von Geusau NJ, Mars RB, Hol-royd CB, Yeung N. Activity in human reward-sensitive brain areas is strongly context dependent. Neuroimage 2005; 25: 1302-1309. [CrossRef]
14. Yacubian J, Gläscher J, Schroeder K, Sommer T, Braus DF, Büchel C. Dissociable systems for gain- and loss-related value predic-tions and errors of prediction in the human brain. J Neurosci 2006; 26: 9530-9537. [CrossRef]
15. Wrase J, Kahnt T, Schlagenhauf F, et al. Different neural systems adjust motor behavior in response to reward and punishment. Neuroimage 2007; 36: 1253-1262. [CrossRef]
16. Mowrer OH. Two-factor learning theory: summary and com- ment. Psychol Rev 1951; 58: 350-354. [CrossRef]
17. Mowrer OH, Lamoreaux RR. Avoidance conditioning and signal duration--a study of secondary motivation and reward. Psych Mono 1942; 54: 1-34. [CrossRef]
18. Dickinson A, Dearing M. Appetitive-aversive interactions and inhibitory processes. In A. Dickinson and R.A. Boakes (Eds). Mechanisms of learning and motivation: A memorial volume to Jerzy Konorski. 1979, pp. 203-231.
19. Solomon RL, Corbit JD. An opponent-process theory of motivation. I. Temporal dynamics of affect. Psych Rev 1974; 81: 119-145. [CrossRef]
20. Solomon RL. The opponent-process theory of acquired motiva-tion: the costs of pleasure and the benefits of pain. Am Psychol 1980; 35: 691-712. [CrossRef]
21. Kim H, Shimojo S, O’Doherty JP. Overlapping responses for the expectation of juice and money rewards in human ventromedial prefrontal cortex. Cereb Cortex 2011; 21: 769-776. [CrossRef]
22. Amsel A. The role of frustrative nonreward in noncontinuous re-ward situations. Psychol Bull 1958; 55: 102-119. [CrossRef]
23. Amsel A. Frustration theory--many years later. Psychol Bull 1992; 112: 396-399. [CrossRef]
24. Abler B, Walter H, Erk S, Kammerer H, Spitzer M. Prediction error as a linear function of reward probability is coded in human nu-cleus accumbens. Neuroimage 2006; 31: 790-5. [CrossRef]
25. Deichmann R, Gottfried JA, Hutton C, Turner R. Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 2003; 19: 430-441. [CrossRef]
26. Penny W, Friston K, Ashburner J, Kiebel S, Nichols T (Eds.) Statisti-cal parametric mapping: the analysis of functional brain images. Elsevier Press, Amsterdam 2006. p. 101-126.
27. Kim H, Shimojo S, O’Doherty JP. Overlapping responses for the expectation of juice and money rewards in human ventromedial prefrontal cortex. Cereb Cortex 2011; 21: 769-776. [CrossRef]
28. Bechara A, Damasio AR, Damasio H, Anderson SW. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 1994; 50: 7-15. [CrossRef]
29. Bechara A, Damasio H, Tranel D, Damasio AR. Deciding advan-tageously before knowing the advantageous strategy. Science 1997; 275: 1293-1295. [CrossRef]
30. Wheeler EZ, Fellows LK. The human ventromedial frontal lobe is critical for learning from negative feedback. Brain 2008; 131: 1323-1331. [CrossRef]
31. Fellows LK, Farah MJ. Dissociable elements of human foresight: a role for the ventromedial frontal lobes in framing the future, but not in discounting future rewards. Neuropsychologia 2005; 43: 1214-1221. [CrossRef]
32. Yacubian J, Gläscher J, Schroeder K, Sommer T, Braus DF, Büchel C. Dissociable systems for gain- and loss-related value predic-tions and errors of prediction in the human brain. J Neurosci 2006; 26: 9530-9537. [CrossRef]
33. Jensen J, McIntosh AR, Crawley AP, Mikulis DJ, Remington G, Ka-pur S. Direct activation of the ventral striatum in anticipation of aversive stimuli. Neuron 2003; 40: 1251-1257. [CrossRef]
34. Levita L, Hare TA, Voss HU, Glover G, Ballon DJ, Casey BJ. The bi-valent side of the nucleus accumbens. Neuroimage 2009; 44: 1178-1187. [CrossRef]
35. Salamone JD. The involvement of nucleus accumbens dopa-mine in appetitive and aversive motivation. Behav Brain Res 1994; 61: 117-133. [CrossRef]
36. Liu X, Hairston J, Schrier M, Fan J. Common and distinct networks underlying reward va1. Rangel A, Camerer C, Montague PR. A framework for studying the neurobiology of value-based decision making. Nat Rev Neu-rosci 2008; 9: 545-556. [CrossRef]
2. Seymour B, Singer T, Dolan R. The neurobiology of punishment. Nat Rev Neurosci 2007; 8: 300-311. [CrossRef] 3. Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA. Tracking the hemodynamic responses to reward and punishment in the stri-atum. J Neurophysiol 2000; 84: 3072-3077. [CrossRef]
4. Delgado MR, Jou RL, Phelps EA. Neural systems underlying aver-sive conditioning in humans with primary and secondary rein-forcers. Front Neurosci 2011; 5: 71. [CrossRef]
5. Jensen J, McIntosh AR, Crawley AP, Mikulis DJ, Remington G, Ka-pur S. Direct activation of the ventral striatum in anticipation of aversive stimuli. Neuron 2003; 40: 1251-1257. [CrossRef]
6. D'Ardenne K, McClure SM, Nystrom LE, Cohen JD. BOLD re-sponses reflecting dopaminergic signals in the human ventral tegmental area. Science 2008; 319: 1264-1267. [CrossRef]
7. Berns GS, McClure SM, Pagnoni G, Montague PR. Predictability modulates human brain response to reward. J Neurosci 2001; 21: 2793-2798. [CrossRef]
8. O’Doherty JP. Reward representations and reward-related learn-ing in the human brain: insights from neuroimaging. Curr Opin Neurobiol 2004; 14: 769-766. [CrossRef]
9. Camara E, Rodriguez-Fornells A, Münte TF. Functional connec-tivity of reward processing in the brain. Front Hum Neurosci 2009; 2: 19. [CrossRef]
10. Camara E, Rodriguez-Fornells A, Ye Z, Münte TF. Reward net-works in the brain as captured by connectivity measures. Front Neurosci 2009; 3: 350-362. [CrossRef]
11. Dreher JC, Grafman J. Dissociating the roles of the rostral anterior cin-gulate and the lateral prefrontal cortices in performing two tasks simul-taneously or successively. Cereb Cortex 2003; 13: 329-339. [CrossRef]
12. Gottfried JA, O’Doherty J, Dolan RJ. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 2003; 301: 1104-1107. [CrossRef]
13. Nieuwenhuis S, Heslenfeld DJ, von Geusau NJ, Mars RB, Hol-royd CB, Yeung N. Activity in human reward-sensitive brain areas is strongly context dependent. Neuroimage 2005; 25: 1302-1309. [CrossRef]
14. Yacubian J, Gläscher J, Schroeder K, Sommer T, Braus DF, Büchel C. Dissociable systems for gain- and loss-related value predic-tions and errors of prediction in the human brain. J Neurosci 2006; 26: 9530-9537. [CrossRef]
15. Wrase J, Kahnt T, Schlagenhauf F, et al. Different neural systems adjust motor behavior in response to reward and punishment. Neuroimage 2007; 36: 1253-1262. [CrossRef]
16. Mowrer OH. Two-factor learning theory: summary and com- ment. Psychol Rev 1951; 58: 350-354. [CrossRef]
17. Mowrer OH, Lamoreaux RR. Avoidance conditioning and signal duration--a study of secondary motivation and reward. Psych Mono 1942; 54: 1-34. [CrossRef]
18. Dickinson A, Dearing M. Appetitive-aversive interactions and inhibitory processes. In A. Dickinson and R.A. Boakes (Eds). Mechanisms of learning and motivation: A memorial volume to Jerzy Konorski. 1979, pp. 203-231.
19. Solomon RL, Corbit JD. An opponent-process theory of motivation. I. Temporal dynamics of affect. Psych Rev 1974; 81: 119-145. [CrossRef]
20. Solomon RL. The opponent-process theory of acquired motiva-tion: the costs of pleasure and the benefits of pain. Am Psychol 1980; 35: 691-712. [CrossRef]
21. Kim H, Shimojo S, O’Doherty JP. Overlapping responses for the expectation of juice and money rewards in human ventromedial prefrontal cortex. Cereb Cortex 2011; 21: 769-776. [CrossRef]
22. Amsel A. The role of frustrative nonreward in noncontinuous re-ward situations. Psychol Bull 1958; 55: 102-119. [CrossRef]
23. Amsel A. Frustration theory--many years later. Psychol Bull 1992; 112: 396-399. [CrossRef]
24. Abler B, Walter H, Erk S, Kammerer H, Spitzer M. Prediction error as a linear function of reward probability is coded in human nu-cleus accumbens. Neuroimage 2006; 31: 790-5. [CrossRef]
25. Deichmann R, Gottfried JA, Hutton C, Turner R. Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 2003; 19: 430-441. [CrossRef]
26. Penny W, Friston K, Ashburner J, Kiebel S, Nichols T (Eds.) Statisti-cal parametric mapping: the analysis of functional brain images. Elsevier Press, Amsterdam 2006. p. 101-126.
27. Kim H, Shimojo S, O’Doherty JP. Overlapping responses for the expectation of juice and money rewards in human ventromedial prefrontal cortex. Cereb Cortex 2011; 21: 769-776. [CrossRef]
28. Bechara A, Damasio AR, Damasio H, Anderson SW. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 1994; 50: 7-15. [CrossRef]
29. Bechara A, Damasio H, Tranel D, Damasio AR. Deciding advan-tageously before knowing the advantageous strategy. Science 1997; 275: 1293-1295. [CrossRef]
30. Wheeler EZ, Fellows LK. The human ventromedial frontal lobe is critical for learning from negative feedback. Brain 2008; 131: 1323-1331. [CrossRef]
31. Fellows LK, Farah MJ. Dissociable elements of human foresight: a role for the ventromedial frontal lobes in framing the future, but not in discounting future rewards. Neuropsychologia 2005; 43: 1214-1221. [CrossRef]
32. Yacubian J, Gläscher J, Schroeder K, Sommer T, Braus DF, Büchel C. Dissociable systems for gain- and loss-related value predic-tions and errors of prediction in the human brain. J Neurosci 2006; 26: 9530-9537. [CrossRef]
33. Jensen J, McIntosh AR, Crawley AP, Mikulis DJ, Remington G, Ka-pur S. Direct activation of the ventral striatum in anticipation of aversive stimuli. Neuron 2003; 40: 1251-1257. [CrossRef]
34. Levita L, Hare TA, Voss HU, Glover G, Ballon DJ, Casey BJ. The bi-valent side of the nucleus accumbens. Neuroimage 2009; 44: 1178-1187. [CrossRef]
35. Salamone JD. The involvement of nucleus accumbens dopa-mine in appetitive and aversive motivation. Behav Brain Res 1994; 61: 117-133. [CrossRef]
36. Liu X, Hairston J, Schrier M, Fan J. Common and distinct networks underlying reward valence and processing stages: a meta-anal- Neurol Sci Neurophysiol 2019; 36(2): 69-77 Neural correlates of opponent processes for financial gains and losses, Erdeniz and Done. ysis of functional neuroimaging studies. Neurosci Biobehav Rev 2011; 35: 1219-1236. [CrossRef]
37. Zink CF, Pagnoni G, Martin ME, Dhamala M, Berns GS. Human striatal response to salient nonrewarding stimuli. J Neurosci-ence 2003; 23: 8092-8097. [CrossRef]
38. Knutson B, Bossaerts P. Neural antecedents of financial deci-sions. J Neuroscience 2007; 27: 8174-8177. [CrossRef]
39. Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD. Dopa-mine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 2006; 442: 1042-1045. [CrossRef]
40. Seymour B, O'Doherty JP, Dayan P, et al. Temporal difference models describe higher-order learning in humans. Nature 2004; 429: 664-667. [CrossRef]
41. Preuschoff K, Bossaerts P, Quartz SR. Neural differentiation of ex-pected reward and risk in human subcortical structures. Neuron 2006; 51: 381-390. [CrossRef]
42. Koch K, Schachtzabel C, Wagner G, Reichenbach JR, Sauer H, Schlösser R. The neural correlates of reward-related trial-and-er- ror learning: an fMRI study with a probabilistic learning task. Learn Mem 2008; 15: 728-732. [CrossRef]lence and processing stages: a meta-anal- Neurol Sci Neurophysiol 2019; 36(2): 69-77 Neural correlates of opponent processes for financial gains and losses, Erdeniz and Done. ysis of functional neuroimaging studies. Neurosci Biobehav Rev 2011; 35: 1219-1236. [CrossRef]
37. Zink CF, Pagnoni G, Martin ME, Dhamala M, Berns GS. Human striatal response to salient nonrewarding stimuli. J Neurosci-ence 2003; 23: 8092-8097. [CrossRef]
38. Knutson B, Bossaerts P. Neural antecedents of financial deci-sions. J Neuroscience 2007; 27: 8174-8177. [CrossRef]
39. Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD. Dopa-mine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 2006; 442: 1042-1045. [CrossRef]
40. Seymour B, O'Doherty JP, Dayan P, et al. Temporal difference models describe higher-order learning in humans. Nature 2004; 429: 664-667. [CrossRef]
41. Preuschoff K, Bossaerts P, Quartz SR. Neural differentiation of ex-pected reward and risk in human subcortical structures. Neuron 2006; 51: 381-390. [CrossRef]
42. Koch K, Schachtzabel C, Wagner G, Reichenbach JR, Sauer H, Schlösser R. The neural correlates of reward-related trial-and-er- ror learning: an fMRI study with a probabilistic learning task. Learn Mem 2008; 15: 728-732. [CrossRef]

APA	ERDENIZ B, Done J (2019). Neural correlates of opponent processes for financial gains and losses. , 69 - 77. 10.5152/NSN.2019.10942
Chicago	ERDENIZ BURAK,Done John Neural correlates of opponent processes for financial gains and losses. (2019): 69 - 77. 10.5152/NSN.2019.10942
MLA	ERDENIZ BURAK,Done John Neural correlates of opponent processes for financial gains and losses. , 2019, ss.69 - 77. 10.5152/NSN.2019.10942
AMA	ERDENIZ B,Done J Neural correlates of opponent processes for financial gains and losses. . 2019; 69 - 77. 10.5152/NSN.2019.10942
Vancouver	ERDENIZ B,Done J Neural correlates of opponent processes for financial gains and losses. . 2019; 69 - 77. 10.5152/NSN.2019.10942
IEEE	ERDENIZ B,Done J "Neural correlates of opponent processes for financial gains and losses." , ss.69 - 77, 2019. 10.5152/NSN.2019.10942
ISNAD	ERDENIZ, BURAK - Done, John. "Neural correlates of opponent processes for financial gains and losses". (2019), 69-77. https://doi.org/10.5152/NSN.2019.10942

APA	ERDENIZ B, Done J (2019). Neural correlates of opponent processes for financial gains and losses. Neurological sciences and neurophysiology (Online), 36(2), 69 - 77. 10.5152/NSN.2019.10942
Chicago	ERDENIZ BURAK,Done John Neural correlates of opponent processes for financial gains and losses. Neurological sciences and neurophysiology (Online) 36, no.2 (2019): 69 - 77. 10.5152/NSN.2019.10942
MLA	ERDENIZ BURAK,Done John Neural correlates of opponent processes for financial gains and losses. Neurological sciences and neurophysiology (Online), vol.36, no.2, 2019, ss.69 - 77. 10.5152/NSN.2019.10942
AMA	ERDENIZ B,Done J Neural correlates of opponent processes for financial gains and losses. Neurological sciences and neurophysiology (Online). 2019; 36(2): 69 - 77. 10.5152/NSN.2019.10942
Vancouver	ERDENIZ B,Done J Neural correlates of opponent processes for financial gains and losses. Neurological sciences and neurophysiology (Online). 2019; 36(2): 69 - 77. 10.5152/NSN.2019.10942
IEEE	ERDENIZ B,Done J "Neural correlates of opponent processes for financial gains and losses." Neurological sciences and neurophysiology (Online), 36, ss.69 - 77, 2019. 10.5152/NSN.2019.10942
ISNAD	ERDENIZ, BURAK - Done, John. "Neural correlates of opponent processes for financial gains and losses". Neurological sciences and neurophysiology (Online) 36/2 (2019), 69-77. https://doi.org/10.5152/NSN.2019.10942