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Short-term temporal discounting of reward value in human ventral striatum.

Gregorios-Pippas L, Tobler PN, Schultz W - J. Neurophysiol. (2009)

Bottom Line: We demonstrated hyperbolic and exponential decreases of striatal responses to reward predicting stimuli within this time range, irrespective of changes in reward rate.These data suggest that delays of a few seconds affect the neural processing of predicted reward value in the ventral striatum and engage the temporal sensitivity of reward responses.Comparisons with electrophysiological animal data suggest that ventral striatal reward discounting may involve dopaminergic and orbitofrontal inputs.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK.

ABSTRACT
Delayed rewards lose their value for economic decisions and constitute weaker reinforcers for learning. Temporal discounting of reward value already occurs within a few seconds in animals, which allows investigations of the underlying neurophysiological mechanisms. However, it is difficult to relate these mechanisms to human discounting behavior, which is usually studied over days and months and may engage different brain processes. Our study aimed to bridge the gap by using very short delays and measuring human functional magnetic resonance responses in one of the key reward centers of the brain, the ventral striatum. We used psychometric methods to assess subjective timing and valuation of monetary rewards with delays of 4.0-13.5 s. We demonstrated hyperbolic and exponential decreases of striatal responses to reward predicting stimuli within this time range, irrespective of changes in reward rate. Lower reward magnitudes induced steeper behavioral and striatal discounting. By contrast, striatal responses following the delivery of reward reflected the uncertainty in subjective timing associated with delayed rewards rather than value discounting. These data suggest that delays of a few seconds affect the neural processing of predicted reward value in the ventral striatum and engage the temporal sensitivity of reward responses. Comparisons with electrophysiological animal data suggest that ventral striatal reward discounting may involve dopaminergic and orbitofrontal inputs.

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BOLD signal discrimination between discounted reward values. A: analysis using receiver operator characteristics (ROC) comparing BOLD responses to stimuli predicting shorter versus longer delays. Curves plot cumulative probabilities of participants showing peak responses that exceed the criterion threshold with longer delays against probabilities with shorter delays. The ROC curve for the seven participants showing strong behavioral discounting was above the diagonal, indicating higher probabilities for shorter compared with longer delays and thus good discrimination (ROC = 0.85; P < 0.01 permutation test), whereas the ROC curve for the 7 nondiscounters approached the diagonal indicating poor discrimination (ROC = 0.57; P = 0.32). Data were averaged across fixed and adjusted ITI schedules and across all 6 possible comparisons (4 vs. 6, 9, and 13.5 s, 6 vs. 9 and 13.5 s, and 9 vs. 13.5 s delays; see Fig. 1B for separate ITI schedules). Measures were from peak voxel of circled area shown in Fig. 3A. B and C: numeric ROC values (area under the curve) for participants showing behavioral discounting (B) and absence of discounting (C). ***P < 0.001, **P < 0.01, *P < 0.05; permutation test. Values <0.5 derive from higher responses to longer compared with shorter delays and were rectified on 0.5 for statistical comparison between discounters and nondiscounters (P = 0.03; Wilcoxon test). ROC analysis comparing discounters vs. nondiscounters resulted in ROC values of 0.743 (4 s), 0.307 (6 s), 0.393 (9 s), 0.300 (13.5 s).
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f4: BOLD signal discrimination between discounted reward values. A: analysis using receiver operator characteristics (ROC) comparing BOLD responses to stimuli predicting shorter versus longer delays. Curves plot cumulative probabilities of participants showing peak responses that exceed the criterion threshold with longer delays against probabilities with shorter delays. The ROC curve for the seven participants showing strong behavioral discounting was above the diagonal, indicating higher probabilities for shorter compared with longer delays and thus good discrimination (ROC = 0.85; P < 0.01 permutation test), whereas the ROC curve for the 7 nondiscounters approached the diagonal indicating poor discrimination (ROC = 0.57; P = 0.32). Data were averaged across fixed and adjusted ITI schedules and across all 6 possible comparisons (4 vs. 6, 9, and 13.5 s, 6 vs. 9 and 13.5 s, and 9 vs. 13.5 s delays; see Fig. 1B for separate ITI schedules). Measures were from peak voxel of circled area shown in Fig. 3A. B and C: numeric ROC values (area under the curve) for participants showing behavioral discounting (B) and absence of discounting (C). ***P < 0.001, **P < 0.01, *P < 0.05; permutation test. Values <0.5 derive from higher responses to longer compared with shorter delays and were rectified on 0.5 for statistical comparison between discounters and nondiscounters (P = 0.03; Wilcoxon test). ROC analysis comparing discounters vs. nondiscounters resulted in ROC values of 0.743 (4 s), 0.307 (6 s), 0.393 (9 s), 0.300 (13.5 s).

Mentions: We next asked to which extent the temporal discounting in the ventral striatum (Fig. 3, C and D) might allow an ideal observer to discriminate between reward delays based on the BOLD responses. We used ROC analyses on averaged BOLD responses across all delay combinations and across the two ITI schedules and found significantly higher probabilities of criterion brain activations with shorter compared with longer delays in discounters (ROC area under the curve P = 0.85; P < 0.01 permutation test) but not in nondiscounters (ROC = 0.57; NS; Fig. 4A). Differences between two individual delays were frequently significant in discounters (Fig. 4B) but rarely so in nondiscounters (Fig. 4C), resulting in overall significantly higher ROC values in discounters compared with nondiscounters (P = 0.03; Mann-Whitney test). Separate analyses of the two ITI schedules revealed also significant discriminations of reward delays and differences between discounters and nondiscounters (4 of 6 ROC areas under the curve at P < 0.05 or P < 0.01 in discounters with each ITI schedule, but only 1 of 6 and 2 of 6 ROCs at P < 0.05 in nondiscounters).


Short-term temporal discounting of reward value in human ventral striatum.

Gregorios-Pippas L, Tobler PN, Schultz W - J. Neurophysiol. (2009)

BOLD signal discrimination between discounted reward values. A: analysis using receiver operator characteristics (ROC) comparing BOLD responses to stimuli predicting shorter versus longer delays. Curves plot cumulative probabilities of participants showing peak responses that exceed the criterion threshold with longer delays against probabilities with shorter delays. The ROC curve for the seven participants showing strong behavioral discounting was above the diagonal, indicating higher probabilities for shorter compared with longer delays and thus good discrimination (ROC = 0.85; P < 0.01 permutation test), whereas the ROC curve for the 7 nondiscounters approached the diagonal indicating poor discrimination (ROC = 0.57; P = 0.32). Data were averaged across fixed and adjusted ITI schedules and across all 6 possible comparisons (4 vs. 6, 9, and 13.5 s, 6 vs. 9 and 13.5 s, and 9 vs. 13.5 s delays; see Fig. 1B for separate ITI schedules). Measures were from peak voxel of circled area shown in Fig. 3A. B and C: numeric ROC values (area under the curve) for participants showing behavioral discounting (B) and absence of discounting (C). ***P < 0.001, **P < 0.01, *P < 0.05; permutation test. Values <0.5 derive from higher responses to longer compared with shorter delays and were rectified on 0.5 for statistical comparison between discounters and nondiscounters (P = 0.03; Wilcoxon test). ROC analysis comparing discounters vs. nondiscounters resulted in ROC values of 0.743 (4 s), 0.307 (6 s), 0.393 (9 s), 0.300 (13.5 s).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2666398&req=5

f4: BOLD signal discrimination between discounted reward values. A: analysis using receiver operator characteristics (ROC) comparing BOLD responses to stimuli predicting shorter versus longer delays. Curves plot cumulative probabilities of participants showing peak responses that exceed the criterion threshold with longer delays against probabilities with shorter delays. The ROC curve for the seven participants showing strong behavioral discounting was above the diagonal, indicating higher probabilities for shorter compared with longer delays and thus good discrimination (ROC = 0.85; P < 0.01 permutation test), whereas the ROC curve for the 7 nondiscounters approached the diagonal indicating poor discrimination (ROC = 0.57; P = 0.32). Data were averaged across fixed and adjusted ITI schedules and across all 6 possible comparisons (4 vs. 6, 9, and 13.5 s, 6 vs. 9 and 13.5 s, and 9 vs. 13.5 s delays; see Fig. 1B for separate ITI schedules). Measures were from peak voxel of circled area shown in Fig. 3A. B and C: numeric ROC values (area under the curve) for participants showing behavioral discounting (B) and absence of discounting (C). ***P < 0.001, **P < 0.01, *P < 0.05; permutation test. Values <0.5 derive from higher responses to longer compared with shorter delays and were rectified on 0.5 for statistical comparison between discounters and nondiscounters (P = 0.03; Wilcoxon test). ROC analysis comparing discounters vs. nondiscounters resulted in ROC values of 0.743 (4 s), 0.307 (6 s), 0.393 (9 s), 0.300 (13.5 s).
Mentions: We next asked to which extent the temporal discounting in the ventral striatum (Fig. 3, C and D) might allow an ideal observer to discriminate between reward delays based on the BOLD responses. We used ROC analyses on averaged BOLD responses across all delay combinations and across the two ITI schedules and found significantly higher probabilities of criterion brain activations with shorter compared with longer delays in discounters (ROC area under the curve P = 0.85; P < 0.01 permutation test) but not in nondiscounters (ROC = 0.57; NS; Fig. 4A). Differences between two individual delays were frequently significant in discounters (Fig. 4B) but rarely so in nondiscounters (Fig. 4C), resulting in overall significantly higher ROC values in discounters compared with nondiscounters (P = 0.03; Mann-Whitney test). Separate analyses of the two ITI schedules revealed also significant discriminations of reward delays and differences between discounters and nondiscounters (4 of 6 ROC areas under the curve at P < 0.05 or P < 0.01 in discounters with each ITI schedule, but only 1 of 6 and 2 of 6 ROCs at P < 0.05 in nondiscounters).

Bottom Line: We demonstrated hyperbolic and exponential decreases of striatal responses to reward predicting stimuli within this time range, irrespective of changes in reward rate.These data suggest that delays of a few seconds affect the neural processing of predicted reward value in the ventral striatum and engage the temporal sensitivity of reward responses.Comparisons with electrophysiological animal data suggest that ventral striatal reward discounting may involve dopaminergic and orbitofrontal inputs.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK.

ABSTRACT
Delayed rewards lose their value for economic decisions and constitute weaker reinforcers for learning. Temporal discounting of reward value already occurs within a few seconds in animals, which allows investigations of the underlying neurophysiological mechanisms. However, it is difficult to relate these mechanisms to human discounting behavior, which is usually studied over days and months and may engage different brain processes. Our study aimed to bridge the gap by using very short delays and measuring human functional magnetic resonance responses in one of the key reward centers of the brain, the ventral striatum. We used psychometric methods to assess subjective timing and valuation of monetary rewards with delays of 4.0-13.5 s. We demonstrated hyperbolic and exponential decreases of striatal responses to reward predicting stimuli within this time range, irrespective of changes in reward rate. Lower reward magnitudes induced steeper behavioral and striatal discounting. By contrast, striatal responses following the delivery of reward reflected the uncertainty in subjective timing associated with delayed rewards rather than value discounting. These data suggest that delays of a few seconds affect the neural processing of predicted reward value in the ventral striatum and engage the temporal sensitivity of reward responses. Comparisons with electrophysiological animal data suggest that ventral striatal reward discounting may involve dopaminergic and orbitofrontal inputs.

Show MeSH
Related in: MedlinePlus