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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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Delay related increase of BOLD responses to reward in left medial striatum. A: anatomical position of increased BOLD response to monetary reward delivered after increasingly longer delays. The activation was significant at P < 0.05 (ventral striatum small volume corrected; peak at –6/12/2). BOLD responses were regressed on the inverse, mean-corrected, actual indifference values of each participant measured in £ during the intertemporal choice task, averaged across fixed and adjusted ITI schedules. B: increase of BOLD responses to monetary reward delivered with increasing delays in the fixed and adjusted ITI schedules, respectively. Fitted curves complied with exponential increases (fixed ITIs: k = 0.33, R2 = 0.97; adjusted ITIs: k = 0.33, R2 = −0.093; P = 0.73 on R2's, Wilcoxon test). C: delay-related increases in BOLD reward responses plotted separately for discounters and nondiscounters. The 2 subgroups were separated according to intertemporal choices following the stimuli, irrespective of processes at the time of reward. Same data as used for B but separated according to the 2 discounting groups. Parameters for exponential curves were for fixed ITIs: discounters: k = 0.45, R2 = 0.95; nondiscounters: k = 0.22, R2 = 0.70; adjusted ITIs: discounters: k = 0.39, R2 = 0.69; nondiscounters: k = 0.16, R2 = 0.74). Despite the apparent differences in fitted exponential curves between discounters and nondiscounters, the differences in fit to the indifference values were insignificant (P = 0.549). In B and C, percent of signal change was measured at peak of time course (4 s after reward) at peak voxel of region shown in A. Delays show PIP estimated values. Data are means ± SE.
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f7: Delay related increase of BOLD responses to reward in left medial striatum. A: anatomical position of increased BOLD response to monetary reward delivered after increasingly longer delays. The activation was significant at P < 0.05 (ventral striatum small volume corrected; peak at –6/12/2). BOLD responses were regressed on the inverse, mean-corrected, actual indifference values of each participant measured in £ during the intertemporal choice task, averaged across fixed and adjusted ITI schedules. B: increase of BOLD responses to monetary reward delivered with increasing delays in the fixed and adjusted ITI schedules, respectively. Fitted curves complied with exponential increases (fixed ITIs: k = 0.33, R2 = 0.97; adjusted ITIs: k = 0.33, R2 = −0.093; P = 0.73 on R2's, Wilcoxon test). C: delay-related increases in BOLD reward responses plotted separately for discounters and nondiscounters. The 2 subgroups were separated according to intertemporal choices following the stimuli, irrespective of processes at the time of reward. Same data as used for B but separated according to the 2 discounting groups. Parameters for exponential curves were for fixed ITIs: discounters: k = 0.45, R2 = 0.95; nondiscounters: k = 0.22, R2 = 0.70; adjusted ITIs: discounters: k = 0.39, R2 = 0.69; nondiscounters: k = 0.16, R2 = 0.74). Despite the apparent differences in fitted exponential curves between discounters and nondiscounters, the differences in fit to the indifference values were insignificant (P = 0.549). In B and C, percent of signal change was measured at peak of time course (4 s after reward) at peak voxel of region shown in A. Delays show PIP estimated values. Data are means ± SE.

Mentions: Given the relationships of BOLD stimulus responses to behavioral discounting, we asked whether BOLD responses to the delivery of reward might reflect similar relationships to subjective reward valuation. We regressed BOLD responses to the reward itself on individual behavioral indifference values and on linear, hyperbolic and exponential functions across the four reward delays. Each of these four regressions identified equally well an area in the ventromedial caudate nucleus in which peaks of reward responses increased with increasing delays in both the fixed and the adjusted ITI schedules (P < 0.05, ventral striatum small volume corrected; Fig. 7A). Correlation coefficients R2 differed slightly but insignificantly between fixed and adjusted ITI schedules (P = 0.73; Wilcoxon test; Fig. 7B). Thus BOLD responses to reward appeared to covary with temporal delays.


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

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

Delay related increase of BOLD responses to reward in left medial striatum. A: anatomical position of increased BOLD response to monetary reward delivered after increasingly longer delays. The activation was significant at P < 0.05 (ventral striatum small volume corrected; peak at –6/12/2). BOLD responses were regressed on the inverse, mean-corrected, actual indifference values of each participant measured in £ during the intertemporal choice task, averaged across fixed and adjusted ITI schedules. B: increase of BOLD responses to monetary reward delivered with increasing delays in the fixed and adjusted ITI schedules, respectively. Fitted curves complied with exponential increases (fixed ITIs: k = 0.33, R2 = 0.97; adjusted ITIs: k = 0.33, R2 = −0.093; P = 0.73 on R2's, Wilcoxon test). C: delay-related increases in BOLD reward responses plotted separately for discounters and nondiscounters. The 2 subgroups were separated according to intertemporal choices following the stimuli, irrespective of processes at the time of reward. Same data as used for B but separated according to the 2 discounting groups. Parameters for exponential curves were for fixed ITIs: discounters: k = 0.45, R2 = 0.95; nondiscounters: k = 0.22, R2 = 0.70; adjusted ITIs: discounters: k = 0.39, R2 = 0.69; nondiscounters: k = 0.16, R2 = 0.74). Despite the apparent differences in fitted exponential curves between discounters and nondiscounters, the differences in fit to the indifference values were insignificant (P = 0.549). In B and C, percent of signal change was measured at peak of time course (4 s after reward) at peak voxel of region shown in A. Delays show PIP estimated values. Data are means ± SE.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f7: Delay related increase of BOLD responses to reward in left medial striatum. A: anatomical position of increased BOLD response to monetary reward delivered after increasingly longer delays. The activation was significant at P < 0.05 (ventral striatum small volume corrected; peak at –6/12/2). BOLD responses were regressed on the inverse, mean-corrected, actual indifference values of each participant measured in £ during the intertemporal choice task, averaged across fixed and adjusted ITI schedules. B: increase of BOLD responses to monetary reward delivered with increasing delays in the fixed and adjusted ITI schedules, respectively. Fitted curves complied with exponential increases (fixed ITIs: k = 0.33, R2 = 0.97; adjusted ITIs: k = 0.33, R2 = −0.093; P = 0.73 on R2's, Wilcoxon test). C: delay-related increases in BOLD reward responses plotted separately for discounters and nondiscounters. The 2 subgroups were separated according to intertemporal choices following the stimuli, irrespective of processes at the time of reward. Same data as used for B but separated according to the 2 discounting groups. Parameters for exponential curves were for fixed ITIs: discounters: k = 0.45, R2 = 0.95; nondiscounters: k = 0.22, R2 = 0.70; adjusted ITIs: discounters: k = 0.39, R2 = 0.69; nondiscounters: k = 0.16, R2 = 0.74). Despite the apparent differences in fitted exponential curves between discounters and nondiscounters, the differences in fit to the indifference values were insignificant (P = 0.549). In B and C, percent of signal change was measured at peak of time course (4 s after reward) at peak voxel of region shown in A. Delays show PIP estimated values. Data are means ± SE.
Mentions: Given the relationships of BOLD stimulus responses to behavioral discounting, we asked whether BOLD responses to the delivery of reward might reflect similar relationships to subjective reward valuation. We regressed BOLD responses to the reward itself on individual behavioral indifference values and on linear, hyperbolic and exponential functions across the four reward delays. Each of these four regressions identified equally well an area in the ventromedial caudate nucleus in which peaks of reward responses increased with increasing delays in both the fixed and the adjusted ITI schedules (P < 0.05, ventral striatum small volume corrected; Fig. 7A). Correlation coefficients R2 differed slightly but insignificantly between fixed and adjusted ITI schedules (P = 0.73; Wilcoxon test; Fig. 7B). Thus BOLD responses to reward appeared to covary with temporal delays.

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