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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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Single participant analyses. A: exponentially fitted decreases of BOLD responses with increasing reward delays in 3 individual participants showing different degrees of behavioral discounting: weak (left), intermediate (middle), and strong (right). Discounting factors k and correlation coefficients R2 were for left: k = 0.00, R2 = 0.00; middle: k = 0.11, R2 = 0.70; right: k = 0.18, R2 = 0.87. For comparison, corresponding hyperbolic values were for left: k = 0.00, R2 = 0.00; middle: k = 0.17, R2 = 0.59; right: k = 0.30, R2 = 0.67 (graphs not shown). B: correlations between BOLD and behavioral discounting for hyperbolically and exponentially fitted data (Pearson correlation on 15 participants). The y axis shows factors from fitted peak BOLD responses of individual participants to the differential reward delay predicting stimuli in the discounting task. The x axis shows behavioral factors from fitted reward values at behavioral choice indifference in the intertemporal choice task using adjusting-amounts and PEST procedures. Discounting factors (k) were averaged across fixed and adjusted ITI schedules. Hyperbolic fits (left): R2 = 0.55 (P < 0.01 against 0 slope); exponential fits (right): R2 = 0.55 (P < 0.001). Measures in A and B were from peak voxel of circled area shown in Fig. 3A.
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f5: Single participant analyses. A: exponentially fitted decreases of BOLD responses with increasing reward delays in 3 individual participants showing different degrees of behavioral discounting: weak (left), intermediate (middle), and strong (right). Discounting factors k and correlation coefficients R2 were for left: k = 0.00, R2 = 0.00; middle: k = 0.11, R2 = 0.70; right: k = 0.18, R2 = 0.87. For comparison, corresponding hyperbolic values were for left: k = 0.00, R2 = 0.00; middle: k = 0.17, R2 = 0.59; right: k = 0.30, R2 = 0.67 (graphs not shown). B: correlations between BOLD and behavioral discounting for hyperbolically and exponentially fitted data (Pearson correlation on 15 participants). The y axis shows factors from fitted peak BOLD responses of individual participants to the differential reward delay predicting stimuli in the discounting task. The x axis shows behavioral factors from fitted reward values at behavioral choice indifference in the intertemporal choice task using adjusting-amounts and PEST procedures. Discounting factors (k) were averaged across fixed and adjusted ITI schedules. Hyperbolic fits (left): R2 = 0.55 (P < 0.01 against 0 slope); exponential fits (right): R2 = 0.55 (P < 0.001). Measures in A and B were from peak voxel of circled area shown in Fig. 3A.

Mentions: The analyses separating discounters from nondiscounters suggested that the decreases of BOLD responses reflected the behavioral discounting of delayed rewards. We investigated the strength of this relationship by analyses on individual participants. The decay of BOLD responses across increasing delays differed substantially between individual participants with different degrees of behavioral discounting. Thus weak discounters showed no decay in BOLD responses, whereas participants with intermediate and strong behavioral discounting showed progressively steeper decreases of BOLD responses (Fig. 5A).


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

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

Single participant analyses. A: exponentially fitted decreases of BOLD responses with increasing reward delays in 3 individual participants showing different degrees of behavioral discounting: weak (left), intermediate (middle), and strong (right). Discounting factors k and correlation coefficients R2 were for left: k = 0.00, R2 = 0.00; middle: k = 0.11, R2 = 0.70; right: k = 0.18, R2 = 0.87. For comparison, corresponding hyperbolic values were for left: k = 0.00, R2 = 0.00; middle: k = 0.17, R2 = 0.59; right: k = 0.30, R2 = 0.67 (graphs not shown). B: correlations between BOLD and behavioral discounting for hyperbolically and exponentially fitted data (Pearson correlation on 15 participants). The y axis shows factors from fitted peak BOLD responses of individual participants to the differential reward delay predicting stimuli in the discounting task. The x axis shows behavioral factors from fitted reward values at behavioral choice indifference in the intertemporal choice task using adjusting-amounts and PEST procedures. Discounting factors (k) were averaged across fixed and adjusted ITI schedules. Hyperbolic fits (left): R2 = 0.55 (P < 0.01 against 0 slope); exponential fits (right): R2 = 0.55 (P < 0.001). Measures in A and B were from peak voxel of circled area shown in Fig. 3A.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f5: Single participant analyses. A: exponentially fitted decreases of BOLD responses with increasing reward delays in 3 individual participants showing different degrees of behavioral discounting: weak (left), intermediate (middle), and strong (right). Discounting factors k and correlation coefficients R2 were for left: k = 0.00, R2 = 0.00; middle: k = 0.11, R2 = 0.70; right: k = 0.18, R2 = 0.87. For comparison, corresponding hyperbolic values were for left: k = 0.00, R2 = 0.00; middle: k = 0.17, R2 = 0.59; right: k = 0.30, R2 = 0.67 (graphs not shown). B: correlations between BOLD and behavioral discounting for hyperbolically and exponentially fitted data (Pearson correlation on 15 participants). The y axis shows factors from fitted peak BOLD responses of individual participants to the differential reward delay predicting stimuli in the discounting task. The x axis shows behavioral factors from fitted reward values at behavioral choice indifference in the intertemporal choice task using adjusting-amounts and PEST procedures. Discounting factors (k) were averaged across fixed and adjusted ITI schedules. Hyperbolic fits (left): R2 = 0.55 (P < 0.01 against 0 slope); exponential fits (right): R2 = 0.55 (P < 0.001). Measures in A and B were from peak voxel of circled area shown in Fig. 3A.
Mentions: The analyses separating discounters from nondiscounters suggested that the decreases of BOLD responses reflected the behavioral discounting of delayed rewards. We investigated the strength of this relationship by analyses on individual participants. The decay of BOLD responses across increasing delays differed substantially between individual participants with different degrees of behavioral discounting. Thus weak discounters showed no decay in BOLD responses, whereas participants with intermediate and strong behavioral discounting showed progressively steeper decreases of BOLD responses (Fig. 5A).

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