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Articles, Behavioral/Systems/Cognitive

Dynamic Fluctuations in Dopamine Efflux in the Prefrontal Cortex and Nucleus Accumbens during Risk-Based Decision Making

Jennifer R. St. Onge, Soyon Ahn, Anthony G. Phillips and Stan B. Floresco
Journal of Neuroscience 21 November 2012, 32 (47) 16880-16891; https://doi.org/10.1523/JNEUROSCI.3807-12.2012
Jennifer R. St. Onge
Department of Psychology and Brain Research Center, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
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Soyon Ahn
Department of Psychology and Brain Research Center, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
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Anthony G. Phillips
Department of Psychology and Brain Research Center, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
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Stan B. Floresco
Department of Psychology and Brain Research Center, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
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  • Figure 1.
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    Figure 1.

    Probabilistic discounting task design. A, Cost/benefit contingencies associated with responding on either lever. B, Format of a single free-choice trial.

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    Figure 2.

    Location of the microdialysis probes in the PFC (top) and NAc (bottom). Vertical lines represent length of the 2 mm dialysis probes.

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    Figure 3.

    Choice behavior and reward data obtained during microdialysis tests. A, Percentage choice of the Large/Risky lever across four blocks of free-choice trials from rats in the PFC groups tested on either the descending (circles, n = 12) or ascending (squares, n = 11) variants of the probabilistic discounting tasks. Choice of the Large/Risky lever (y-axis) is plotted as a function of the Large/Risky reward probability by block (x-axis) in the manner in which reward probabilities changed for the different groups. B, Choice data displayed by rats in the NAc groups (descending, n = 13; ascending, n = 10). C, Choice data averaged across descending and ascending variants of the probabilistic discounting task for rats in the PFC (squares) and NAc (circles) groups. D, The amount of reward pellets obtained over the different probability blocks for rats in the PFC and NAc groups tested on either the probabilistic discounting or yoked-reward tasks. Note that animals obtained a substantially greater number of pellets in the 100% and 50% blocks compared with the other blocks.

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    Figure 4.

    Fluctuations in PFC DA efflux during decision making track changes in the relative rate of reward received. A, Percentage change in basal DA extracellular levels in the PFC for rats trained on the descending (yellow circles, n = 12) and ascending (blue circles, n = 11) variants of the probabilistic discounting task, plotted as a function of 7 min sample number. Star denotes p < 0.01 versus baseline for all samples in both groups. Rats tested on the descending version displayed an initial increase in DA that diminished as Large/Risky reward probabilities decreased, whereas those trained on the ascending version showed the opposite profile. B, Change in PFC DA efflux for all rats trained on the both variants of the probabilistic discounting task (circles, n = 23) plotted as a function of probability block. Gray and green circles correspond to DA levels obtained during forced- and free-choice portions of each block. Combined data from rats in the yoked-reward experiment (squares, n = 18) are also plotted. Cross denotes p < 0.05 significant difference in DA from samples obtained during the 25% and 12.5% blocks, relative to the 100% and 50% blocks for both groups.

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    Figure 5.

    Fluctuations in NAc DA efflux track multiple factors related to decision making. A, Percentage change in basal DA extracellular efflux in the NAc for rats trained on the descending (yellow circles, n = 13) and ascending (blue circles, n = 10) variants of the probabilistic discounting task, plotted as a function of sample number. All other conventions are the same as Figure 4A. B, Change in NAc DA efflux for all rats trained on both variants of the probabilistic discounting task (n = 23), plotted as a function of probability block. All other conventions are the same as Figure 4B. DA levels during probabilistic discounting did not differ across the 100% to 25% blocks (n.s.), whereas levels during the 12.5% block were significantly lower than the other three blocks (p < 0.05, denoted by the dagger). Note the sawtooth pattern of change during the discounting task, where DA levels tended to be higher during free-choice (green circles) versus force-choice (gray circles) trials. Squares represent combined data from rats in the yoked-reward experiments (n = 15). Cross denotes p < 0.05 significant difference in DA from samples obtained during the 50%, 25%, and 12.5% blocks, relative to the 100% blocks for rats in the yoked-reward groups. Dashed outline highlights data points used for a targeted analysis comparing DA levels during the discounting versus yoked-reward conditions (averaged in E) C, Percentage change in NAc DA efflux displayed by rats in the yoked experiments that received reward schedules matched to subjects trained on the descending (yellow triangles, n = 8) and ascending (blue triangles, n = 7) variants of the discounting task. Star denotes significant difference at p < 0.05 versus baseline. Cross denotes p < 0.05 for a particular sample in the descending group compared with a sample obtained from the ascending group during the equivalent probability block. All other conventions are the same as Figure 5A. D, Average change NAc DA concentrations obtained during forced-choice (gray bar) and free-choice (green bar) portions of the discounting task. E, Average DA levels relative to baseline taken from the 50–12.5% blocks (highlighted in B) from all rats in the discounting and yoked-reward experiments. During this portion of the tasks, DA levels were higher in rats performing the discounting task (p < 0.05, star) compared with those receiving a comparable schedule of reward, but not making decisions.

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    Figure 6.

    Comparison of changes in choice biases, reward rates, and DA efflux in the PFC and NAc. Graphs depict change scores relative to the 100% block for DA concentration during free-choice blocks (circles), choice of the Large/Risky option (diamonds), and the amount of food reward received (triangles). Lines display the relative slopes for each of the curves. A, Changes in DA efflux in the PFC during decision making closely corresponded to changes in the amount of food reward received across blocks, as the slopes of these two curves were not significantly different (n.s.). In contrast, changes in risky choice occurred at a significantly slower rate (p < 0.05, star). B, Changes in DA efflux in the NAc closely tracked changes in choice behavior across blocks (n.s.), but not reward rates (p < 0.05, star).

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    Figure 7.

    Changes in response latencies across probability blocks. Graph depicts latencies to response during forced-choice (open circles), free-choice (gray circles), and average of the two values (squares), plotted as a function of probability block, for rats with microdialysis probes in the PFC (A) and the NAc (B).

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    Table 1.

    Mean response latency (in seconds) and trial omission data recorded while animals performed the descending and ascending versions of the probabilistic discounting task during medial PFC and NAc microdialysis tests

    Response latencyTrial omissions
    PFC
        Descending probabilistic discounting0.59 (0.09)0.42 (0.19)
        Ascending probabilistic discounting0.43 (0.06)1.09 (0.34)
    NAc
        Descending probabilistic discounting0.66 (0.13)1.58 (1.10)
        Ascending probabilistic discounting0.46 (0.07)2.10 (0.78)
    • Values are displayed as mean (SEM).

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The Journal of Neuroscience: 32 (47)
Journal of Neuroscience
Vol. 32, Issue 47
21 Nov 2012
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Dynamic Fluctuations in Dopamine Efflux in the Prefrontal Cortex and Nucleus Accumbens during Risk-Based Decision Making
Jennifer R. St. Onge, Soyon Ahn, Anthony G. Phillips, Stan B. Floresco
Journal of Neuroscience 21 November 2012, 32 (47) 16880-16891; DOI: 10.1523/JNEUROSCI.3807-12.2012

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Dynamic Fluctuations in Dopamine Efflux in the Prefrontal Cortex and Nucleus Accumbens during Risk-Based Decision Making
Jennifer R. St. Onge, Soyon Ahn, Anthony G. Phillips, Stan B. Floresco
Journal of Neuroscience 21 November 2012, 32 (47) 16880-16891; DOI: 10.1523/JNEUROSCI.3807-12.2012
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