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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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Influence of reward magnitude and personal assets on decreases of BOLD responses during temporal discounting. A: anatomical position of ventral striatum BOLD response to reward delay predicting stimuli showing significantly different discounting between 5 and 20 £ rewards (P < 0.02; ventral striatum small volume corrected; peak voxel at −8/16/-8). This experiment employed only 3 reward delays (4, 8, and 12 s) and fixed ITIs. The linear regression used the subjective delays from the PIP task and an exponential discounting factor of k = 0.06. B: steeper decreases of peak BOLD responses to reward delay predicting stimuli during temporal discounting with lower objective reward magnitude. Responses were measured at peak of temporal response at 4 s after stimuli and at peak voxel of region shown in A. Fitted curves are top: hyperbolic functions: discounters: k = 0.26 and k = 0.10 and R2 = 0.67 and R2 = 0.92 for 5 and 20 £, respectively; nondiscounters: k = 0.25 and k = 0.01 and R2 = 0.68 and R2 = 0.004 for 5 and 20 £, respectively; bottom: exponential functions: discounters: k = 0.15 and k = 0.007 and R2 = 0.88 and R2 = 0.98 for 5 and 20 £, respectively; nondiscounters: k = 0.14 and k = 0.005 and R2 = 0.83 and R2 = 0.003 for 5 and 20 £, respectively; data points are means ± SE. C: focus in ventral striatum showing significantly steeper decreases of BOLD responses to reward delay predicting stimuli in participants with higher personal assets. The linear regression tested for differences in exponential discounting between 4 and 13.5 s as function of assets, irrespective of positive or negative slopes of discounting relative to assets. The activation was significant at P < 0.05 (peak at −12/6/-8; small volume corrected for 10-mm sphere around the peak of activation shown in Fig. 3A, −18/14/-8). Regressions were also significant when testing with hyperbolic instead of exponential discounting (P < 0.05, ventral striatum small volume corrected) and when using the actual indifference reward values from each participant obtained in the intertemporal choice task (P < 0.05 uncorrected). D: correlation between contrast estimates of peak BOLD responses and assets from individual participants in the peak voxel of ventral striatal region shown in C. Ventral striatal reward discounting covaried positively with assets for 13.5-s delays in discounters (P = 0.002, R2 = 0.79; Pearson coefficient) but not in nondiscounters (P = 0.06, R2 = 0.53). These relationships varied inconsistently with 4-s delays (discounters: P = 0.11, R2 = 0.37; nondiscounters: P = 0.005, R2 = 0.77). Effects differed insignificantly between 4 and 13.5 s (discounters P = 0.26; nondiscounters: P = 0.53; z test). Contrast estimates reflect the fit with linear combination of regressors.
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f6: Influence of reward magnitude and personal assets on decreases of BOLD responses during temporal discounting. A: anatomical position of ventral striatum BOLD response to reward delay predicting stimuli showing significantly different discounting between 5 and 20 £ rewards (P < 0.02; ventral striatum small volume corrected; peak voxel at −8/16/-8). This experiment employed only 3 reward delays (4, 8, and 12 s) and fixed ITIs. The linear regression used the subjective delays from the PIP task and an exponential discounting factor of k = 0.06. B: steeper decreases of peak BOLD responses to reward delay predicting stimuli during temporal discounting with lower objective reward magnitude. Responses were measured at peak of temporal response at 4 s after stimuli and at peak voxel of region shown in A. Fitted curves are top: hyperbolic functions: discounters: k = 0.26 and k = 0.10 and R2 = 0.67 and R2 = 0.92 for 5 and 20 £, respectively; nondiscounters: k = 0.25 and k = 0.01 and R2 = 0.68 and R2 = 0.004 for 5 and 20 £, respectively; bottom: exponential functions: discounters: k = 0.15 and k = 0.007 and R2 = 0.88 and R2 = 0.98 for 5 and 20 £, respectively; nondiscounters: k = 0.14 and k = 0.005 and R2 = 0.83 and R2 = 0.003 for 5 and 20 £, respectively; data points are means ± SE. C: focus in ventral striatum showing significantly steeper decreases of BOLD responses to reward delay predicting stimuli in participants with higher personal assets. The linear regression tested for differences in exponential discounting between 4 and 13.5 s as function of assets, irrespective of positive or negative slopes of discounting relative to assets. The activation was significant at P < 0.05 (peak at −12/6/-8; small volume corrected for 10-mm sphere around the peak of activation shown in Fig. 3A, −18/14/-8). Regressions were also significant when testing with hyperbolic instead of exponential discounting (P < 0.05, ventral striatum small volume corrected) and when using the actual indifference reward values from each participant obtained in the intertemporal choice task (P < 0.05 uncorrected). D: correlation between contrast estimates of peak BOLD responses and assets from individual participants in the peak voxel of ventral striatal region shown in C. Ventral striatal reward discounting covaried positively with assets for 13.5-s delays in discounters (P = 0.002, R2 = 0.79; Pearson coefficient) but not in nondiscounters (P = 0.06, R2 = 0.53). These relationships varied inconsistently with 4-s delays (discounters: P = 0.11, R2 = 0.37; nondiscounters: P = 0.005, R2 = 0.77). Effects differed insignificantly between 4 and 13.5 s (discounters P = 0.26; nondiscounters: P = 0.53; z test). Contrast estimates reflect the fit with linear combination of regressors.

Mentions: The magnitude of reward influences behavioral discounting rates and lower compared with higher magnitudes are associated with steeper discounting (Kirby and Marakovic 1995). We investigated the effects of reward magnitude on the decreases of BOLD responses in the separate group of 13 participants, using three delays of 4, 8, and 12 s and presenting £ 5 notes in random alternation with £ 20 notes for each delay. Although these participants did not undergo the PEST procedure, their pleasantness ratings suggested significantly stronger temporal discounting for £ 5 compared with £ 20 [hyperbolic: k(£5) = 0.09, k(£20) = 0.04; P < 0.02, Wilcoxon test; exponential: k(£5) = 0.06, k(£20) = 0.04; P < 0.01). Their BOLD responses showed higher hyperbolic and exponential mean discounting factors k for the £ 5 note (k = 0.227, R2 = 0.63 and k = 0.132, R2 = 0.86, respectively) compared with the £ 20 note (k = 0.075, R2 = 0.72 and k = 0.055, R2 = 0.69, respectively). These differences were significant in group comparisons for each discounting function with discounters and nondiscounters pooled (P = 0.04; Wilcoxon test). For further analysis, we separated this group into six discounters and six nondiscounters based on median split of Kendall's tau obtained from the pleasantness ratings averaged over £ 5 and £ 20. The group of discounters showed substantially steeper, delay related decreases of BOLD responses for £ 5 compared with £ 20 (hyperbolic: P = 0.035; exponential: P = 0.068; Wilcoxon test; Fig. 6, A and B). Nondiscounters showed no BOLD decreases with £ 20 and only slight decreases with £ 5 (hyperbolic: P = 0.46; exponential: P = 0.34). Thus compatible with notions on behavioral discounting, lower compared with higher reward magnitudes appeared to be associated with steeper decreases of BOLD responses to delay predicting stimuli at delays of seconds.


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

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

Influence of reward magnitude and personal assets on decreases of BOLD responses during temporal discounting. A: anatomical position of ventral striatum BOLD response to reward delay predicting stimuli showing significantly different discounting between 5 and 20 £ rewards (P < 0.02; ventral striatum small volume corrected; peak voxel at −8/16/-8). This experiment employed only 3 reward delays (4, 8, and 12 s) and fixed ITIs. The linear regression used the subjective delays from the PIP task and an exponential discounting factor of k = 0.06. B: steeper decreases of peak BOLD responses to reward delay predicting stimuli during temporal discounting with lower objective reward magnitude. Responses were measured at peak of temporal response at 4 s after stimuli and at peak voxel of region shown in A. Fitted curves are top: hyperbolic functions: discounters: k = 0.26 and k = 0.10 and R2 = 0.67 and R2 = 0.92 for 5 and 20 £, respectively; nondiscounters: k = 0.25 and k = 0.01 and R2 = 0.68 and R2 = 0.004 for 5 and 20 £, respectively; bottom: exponential functions: discounters: k = 0.15 and k = 0.007 and R2 = 0.88 and R2 = 0.98 for 5 and 20 £, respectively; nondiscounters: k = 0.14 and k = 0.005 and R2 = 0.83 and R2 = 0.003 for 5 and 20 £, respectively; data points are means ± SE. C: focus in ventral striatum showing significantly steeper decreases of BOLD responses to reward delay predicting stimuli in participants with higher personal assets. The linear regression tested for differences in exponential discounting between 4 and 13.5 s as function of assets, irrespective of positive or negative slopes of discounting relative to assets. The activation was significant at P < 0.05 (peak at −12/6/-8; small volume corrected for 10-mm sphere around the peak of activation shown in Fig. 3A, −18/14/-8). Regressions were also significant when testing with hyperbolic instead of exponential discounting (P < 0.05, ventral striatum small volume corrected) and when using the actual indifference reward values from each participant obtained in the intertemporal choice task (P < 0.05 uncorrected). D: correlation between contrast estimates of peak BOLD responses and assets from individual participants in the peak voxel of ventral striatal region shown in C. Ventral striatal reward discounting covaried positively with assets for 13.5-s delays in discounters (P = 0.002, R2 = 0.79; Pearson coefficient) but not in nondiscounters (P = 0.06, R2 = 0.53). These relationships varied inconsistently with 4-s delays (discounters: P = 0.11, R2 = 0.37; nondiscounters: P = 0.005, R2 = 0.77). Effects differed insignificantly between 4 and 13.5 s (discounters P = 0.26; nondiscounters: P = 0.53; z test). Contrast estimates reflect the fit with linear combination of regressors.
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f6: Influence of reward magnitude and personal assets on decreases of BOLD responses during temporal discounting. A: anatomical position of ventral striatum BOLD response to reward delay predicting stimuli showing significantly different discounting between 5 and 20 £ rewards (P < 0.02; ventral striatum small volume corrected; peak voxel at −8/16/-8). This experiment employed only 3 reward delays (4, 8, and 12 s) and fixed ITIs. The linear regression used the subjective delays from the PIP task and an exponential discounting factor of k = 0.06. B: steeper decreases of peak BOLD responses to reward delay predicting stimuli during temporal discounting with lower objective reward magnitude. Responses were measured at peak of temporal response at 4 s after stimuli and at peak voxel of region shown in A. Fitted curves are top: hyperbolic functions: discounters: k = 0.26 and k = 0.10 and R2 = 0.67 and R2 = 0.92 for 5 and 20 £, respectively; nondiscounters: k = 0.25 and k = 0.01 and R2 = 0.68 and R2 = 0.004 for 5 and 20 £, respectively; bottom: exponential functions: discounters: k = 0.15 and k = 0.007 and R2 = 0.88 and R2 = 0.98 for 5 and 20 £, respectively; nondiscounters: k = 0.14 and k = 0.005 and R2 = 0.83 and R2 = 0.003 for 5 and 20 £, respectively; data points are means ± SE. C: focus in ventral striatum showing significantly steeper decreases of BOLD responses to reward delay predicting stimuli in participants with higher personal assets. The linear regression tested for differences in exponential discounting between 4 and 13.5 s as function of assets, irrespective of positive or negative slopes of discounting relative to assets. The activation was significant at P < 0.05 (peak at −12/6/-8; small volume corrected for 10-mm sphere around the peak of activation shown in Fig. 3A, −18/14/-8). Regressions were also significant when testing with hyperbolic instead of exponential discounting (P < 0.05, ventral striatum small volume corrected) and when using the actual indifference reward values from each participant obtained in the intertemporal choice task (P < 0.05 uncorrected). D: correlation between contrast estimates of peak BOLD responses and assets from individual participants in the peak voxel of ventral striatal region shown in C. Ventral striatal reward discounting covaried positively with assets for 13.5-s delays in discounters (P = 0.002, R2 = 0.79; Pearson coefficient) but not in nondiscounters (P = 0.06, R2 = 0.53). These relationships varied inconsistently with 4-s delays (discounters: P = 0.11, R2 = 0.37; nondiscounters: P = 0.005, R2 = 0.77). Effects differed insignificantly between 4 and 13.5 s (discounters P = 0.26; nondiscounters: P = 0.53; z test). Contrast estimates reflect the fit with linear combination of regressors.
Mentions: The magnitude of reward influences behavioral discounting rates and lower compared with higher magnitudes are associated with steeper discounting (Kirby and Marakovic 1995). We investigated the effects of reward magnitude on the decreases of BOLD responses in the separate group of 13 participants, using three delays of 4, 8, and 12 s and presenting £ 5 notes in random alternation with £ 20 notes for each delay. Although these participants did not undergo the PEST procedure, their pleasantness ratings suggested significantly stronger temporal discounting for £ 5 compared with £ 20 [hyperbolic: k(£5) = 0.09, k(£20) = 0.04; P < 0.02, Wilcoxon test; exponential: k(£5) = 0.06, k(£20) = 0.04; P < 0.01). Their BOLD responses showed higher hyperbolic and exponential mean discounting factors k for the £ 5 note (k = 0.227, R2 = 0.63 and k = 0.132, R2 = 0.86, respectively) compared with the £ 20 note (k = 0.075, R2 = 0.72 and k = 0.055, R2 = 0.69, respectively). These differences were significant in group comparisons for each discounting function with discounters and nondiscounters pooled (P = 0.04; Wilcoxon test). For further analysis, we separated this group into six discounters and six nondiscounters based on median split of Kendall's tau obtained from the pleasantness ratings averaged over £ 5 and £ 20. The group of discounters showed substantially steeper, delay related decreases of BOLD responses for £ 5 compared with £ 20 (hyperbolic: P = 0.035; exponential: P = 0.068; Wilcoxon test; Fig. 6, A and B). Nondiscounters showed no BOLD decreases with £ 20 and only slight decreases with £ 5 (hyperbolic: P = 0.46; exponential: P = 0.34). Thus compatible with notions on behavioral discounting, lower compared with higher reward magnitudes appeared to be associated with steeper decreases of BOLD responses to delay predicting stimuli at delays of seconds.

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