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Articles, Behavioral/Systems/Cognitive

Influence of Reward Delays on Responses of Dopamine Neurons

Shunsuke Kobayashi and Wolfram Schultz
Journal of Neuroscience 30 July 2008, 28 (31) 7837-7846; DOI: https://doi.org/10.1523/JNEUROSCI.1600-08.2008
Shunsuke Kobayashi
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Wolfram Schultz
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    Figure 1.

    Experimental design. A, Intertemporal choice task used for behavioral testing. The animal chooses between an SS reward and an LL reward. The delay of SS and magnitude of LL were fixed. The delay of LL and magnitude of SS varied across blocks of trials. B, Pavlovian task used for dopamine recording. The delay of reward, which varied in every trial, was predicted by a conditioned stimulus (CS).

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    Figure 2.

    Impact of delay and magnitude of reward on choice behavior. A, C, Rate of choosing SS reward as a function of its magnitude for each animal (A, animal A; C, animal B). The magnitude of SS is plotted in percentage volume of LL reward (abscissa). The length of LL delay changed across blocks of trials (red square, 16 s: green triangle, 8 s; blue circle, 4 s; black diamond, 2 s). Curves are best-fit cumulative Weibull functions for each LL delay. Error bars represent SEM. B, D, Hyperbolic model that produces the least-squares error in fitting of the choice behavior (A, C). Value discounting (V, ordinate) is estimated relative to SS reward as a hyperbolic function of delay (t, abscissa). Because SS reward was delayed 0 s (animal A) and 2 s (animal B) from stimulus onset, the ordinate value is 100% at 0 s (B) and 2 s (D). E, Model fitting of behavioral choice based on individual testing sessions. Different combinations of SS and LL were tested in a set of blocks (animal A, 9 sets × 12 different blocks; animal B, 14 sets × 16 different blocks). Goodness of fit (R2) of each series of datasets to hyperbolic (abscissa) and exponential (ordinate) discounting models is plotted (circles, animal A; squares, animal B; see Materials and Methods).

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    Figure 3.

    Probability of licking during a pavlovian task. Probability of licking of each animal is plotted as a function of time from the stimulus onset for each delay condition (2, 4, 8, and 16 s, thick black line to thinner gray lines in this order; no-reward condition, black dotted line). Triangles above indicate the onsets of reward.

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    Figure 4.

    Example dopamine activity during a pavlovian paradigm with variable delay. Activity from a single dopamine neuron recorded from animal A is aligned to stimulus (left) and reward (right) onsets for each delay condition. For each raster plot, the sequence of trials runs from top to bottom. Black tick marks show times of neuronal impulses. Histograms show mean discharge rate in each condition. Stimulus response was generally smaller for instruction of longer delay of reward (delay conditions of 2, 4, 8, and 16 s displayed in the top 4 panels in this order). The panel labeled “free reward” is from the condition in which reward was given without prediction; hence, only reward response is displayed. The panel labeled “no reward” is from the condition in which a stimulus predicted no reward; hence, only stimulus response is displayed.

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    Figure 5.

    The effects of reward delay on population-averaged activity of dopamine neurons. A, C, Mean firing rate for each delay condition was averaged across the population of dopamine neurons from each animal (A, animal A, n = 54; C, animal B, n = 33), aligned to stimulus (left) and reward (right) onsets (solid black line, 2 s delay; dotted black line, 4 s delay; dotted gray line, 8 s delay; solid gray line, 16 s delay). B, D, Correlation coefficient between delay and dopamine activity in a sliding time window (25 ms wide window moved in 5 ms steps) was averaged across the population of dopamine neurons for each animal (B, animal A; D, animal B) as a function of time from stimulus (left) and reward (right) onsets. Shading represents SEM. Dotted lines indicate confidence interval of p < 0.99 based on permutation tests.

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    Figure 6.

    Hyperbolic effect of delay on dopamine activity. A, Goodness of fit (R2) of stimulus response of dopamine neurons to hyperbolic (abscissa) and exponential (ordinate) models. Each symbol corresponds to data from a single neuron (black, activity that fits better to the hyperbolic model; gray, activity that fits better to the exponential model) from two monkeys (circles, animal A; squares, animal B). Most activities were plotted below the unit line, as shown in the inset histogram, indicating better fit to the hyperbolic model as a whole. B, C, Stimulus response was normalized with reference to baseline activity and averaged across the population for each animal (B, animal A; C, animal B). Two different magnitudes of reward were tested with animal A, and large reward was tested with animal B (black squares, large reward; gray circles, small reward). Response to free reward is plotted at zero delay, and response to the stimulus associated with no reward is plotted on the right (CS−). Error bars represent SEM. The best-fit hyperbolic curve is shown for each magnitude of reward (black solid line, large reward; gray dotted line, small reward) with confidence interval of the model (p < 0.95; shading). D, R2 of fitting reward response of dopamine neurons into hyperbolic (abscissa) and exponential (ordinate) models (black, activities that fits better to the hyperbolic model; gray, activity that fits better to the exponential model; circle, animal A; square, animal B). E, F, Population-averaged normalized reward response is shown for animal A (E) and animal B (F). Conventions for different reward magnitudes are the same as in B and C. Error bars represent SEM. The curves show the best-fit hyperbolic function for each magnitude of reward.

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    Figure 7.

    Histologically reconstructed positions of dopamine neurons from monkey B. Rate of discounting of stimulus response (governed by the k value in a hyperbolic function) is denoted by symbols (see inset and Materials and Methods). Neurons recorded from both hemispheres are superimposed. SNc, Substantia nigra pars compacta; SNr, substantia nigra pars reticulata; Ant 8.0–12.0, levels anterior to the interaural stereotaxic line.

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The Journal of Neuroscience: 28 (31)
Journal of Neuroscience
Vol. 28, Issue 31
30 Jul 2008
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Influence of Reward Delays on Responses of Dopamine Neurons
Shunsuke Kobayashi, Wolfram Schultz
Journal of Neuroscience 30 July 2008, 28 (31) 7837-7846; DOI: 10.1523/JNEUROSCI.1600-08.2008

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Influence of Reward Delays on Responses of Dopamine Neurons
Shunsuke Kobayashi, Wolfram Schultz
Journal of Neuroscience 30 July 2008, 28 (31) 7837-7846; DOI: 10.1523/JNEUROSCI.1600-08.2008
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