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Articles, Behavioral/Systems/Cognitive

Serotonin Selectively Modulates Reward Value in Human Decision-Making

Ben Seymour, Nathaniel D. Daw, Jonathan P. Roiser, Peter Dayan and Ray Dolan
Journal of Neuroscience 25 April 2012, 32 (17) 5833-5842; DOI: https://doi.org/10.1523/JNEUROSCI.0053-12.2012
Ben Seymour
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Nathaniel D. Daw
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Jonathan P. Roiser
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Peter Dayan
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Ray Dolan
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  • Figure 1.
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    Figure 1.

    Task design. a, Subjects were required to pick one of four options on each trial. Three seconds after selection, the option yield and outcome that included possible reward (20p) or punishment (painful shock) was given. b, Exemplar graph for one option indicating that the probability of reward and punishment was independent and varied slowly over trials. All options were independent of each other. Outcomes were delivered simultaneously and followed by a variable intertrial interval of 2–6 s.

  • Figure 2.
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    Figure 2.

    a, b, Pre-ingestion (a) and 5 h post-ingestion (b) of serum Tryp:LNAA in the TRP+ (Control) and TRP− (Depleted) groups. c, Current—VAS responses showing a statistically fit sigmoid response function and estimated current intensity for VAS = 8 in an example subject.

  • Figure 3.
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    Figure 3.

    Behavioral results. a, Probability (frequency/total number of trials) of repeating a choice on a particular option given any outcome (All) and given each of the four possible outcomes: reward alone (Rew), pain alone (Pain), reward and pain (Both), and neither reward nor pain (Neither). b, Independent decision weights in TRP+ and TRP− groups. This shows the weights by which rewards, punishments, or previous choices governed the tendency to repeat the same option. Subjects were on average more sensitive to rewards (20p) than punishments (painful shock). c, Decision weights parameterised as exponential kernels, which is equivalent to a truncated reinforcement learning model. Parameter estimates were TRP+ reward sensitivity = 4.18, punishment sensitivity = −2.29, choice repetition (perseveration) = 0.79, TRP− reward sensitivity = 2.50, punishment sensitivity = −2.43, choice repetition = 1.90. d, e, Correlation between change in serum tryptophan:large neutral amino acid ratio at 5 h post-amino acid ingestion and the parameters for reward sensitivity (r = 0.50, p < 0.005; d) and choice perseveration (r = −0.41, p < 0.01; e).

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    Figure 4.

    Neuroimaging results: choice values and choice perseveration. a, BOLD responses corresponding to reward value and avoidance value (thresholded at p < 0.01 × p < 0.01 for display) in ventromedial prefrontal cortex 2, 38, −12 (circled)—our region of a priori interest. Note that both appetitive and avoidance values individually satisfy correction for multiple comparisons in this region (FWE ROI p < 0.05, see Materials and Methods). b, BOLD responses corresponding to covariation of reward value and change in serum tryptophan: long chain amino acid ratio following amino acid ingestion, threshold p < 0.005 for illustration (FWE ROI p < 0.05), showing response in ventromedial prefrontal cortex 12 44 −8 (z = 3.52). c, BOLD responses corresponding to covariation of choice kernel and change in serum tryptophan: long chain amino acid ratio following amino acid ingestion, threshold p < 0.005 for illustration, showing responses in right head of caudate (18, 4, 14; FWE p < 0.05 whole brain) and right anterior pole (16, 66, 14).

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    Figure 5.

    Neuroimaging results: prediction error. a, Overlapping reward and punishment avoidance prediction errors (exclusively masked, p < 0.01 × p < 0.01 for illustration) showing activity in right medial head of caudate (10, 12, 6) and right dorsolateral putamen (28, 0, 6). The appetitive and avoidance prediction error responses are individually significant at FWE ROI p < 0.05 b, Reward prediction errors modulated by serum ΔTRP:ΣLNAA (covariate regression, p < 0.001 uncorrected for display; 34, −4, 4; FWE ROI p < 0.05).

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    Table 1.

    Amino acids constituents by mass

    Isoleucine4.2 g
    Leucine6.6 g
    Lysine4.8 g
    Methionine1.5 g
    Phenylalanine6.6 g
    Threonine3.0 g
    Valine4.8 g
    Tryptophan or placebo3 or 0 g
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    Table 2.

    Bond and Larder scale (1974)

    Alert/Drowsy
    Calm/Excited
    Strong/Feeble
    Clear-Headed/Muzzy
    Well-coordinated/Clumsy
    Energetic/Lethargic
    Contented/Discontented
    Tranquil/Troubled
    Quick-witted/Mentally slow
    Relaxed/Tense
    Attentive/Dreamy
    Proficient/Incompetent
    Happy/Sad
    Amicable/Antagonistic
    Interested/Bored
    Gregarious/Withdrawn
    • View popup
    Table 3.

    BOLD results

    Reward valuep < 0.001 (uncorrected)
        Medial prefrontal cortex−4, 54, −8 (z = 3.74); FWE p < 0.05 SVC
        Bilateral head of caudate14, 2, 16 (z = 4.12); −8, 0, 14 (z = 4.05)
        Anterior cingulate cortex2, 44, 12 (z = 3.72)
        Right lateral orbitofrontal cortex44, 54, −8 (z = 4.35)
    Avoidance valuep < 0.001 (uncorrected)
        Medial prefrontal cortex4, 36, −8 (z = 3.40); FWE p < 0.05 SVC
        Nucleus accumbens−4, 4, −10 (z = 4.56)
        Secondary somatosensory cortex/posterior insula−52, 20, 12 (z = 5.45); −38, −12, 16 (z = 5.16)
        Precuneus−14, −60, 18 (z = 4.97)
        Posterior parietal cortex0, −26, 52 (z = 4.66)
    Overlapping avoidance and reward value
        Ventromedial prefrontal cortex2, 38, −12; −6, 52, −8; −6, 28, −12
        Dorsomedial prefrontal cortex2, 60, 24; 16, 58, 34; −18, 60, 22; −16, 66, 14
        Left posterior insula−56, −2, 0
        Bilateral head of caudate12, 2, 16; −8, 2, 16
        Medial parietal cortex2, −20, 44
        Precuneus−8, −46, 34
    Reward × serotonin (ΔTRP:ΣLNAA)p < 0.001 (uncorrected)
        Ventromedial prefrontal cortex12, 44, −8 (z = 3.52); FWE p < 0.05 SVC
        Left anterior insula−54, 16, 6 (z = 3.84)
        Precuneus16, −54, 28 (z = 3.23)
    Reward prediction errorp < 0.001 (uncorrected)
        Bilateral head of caudate12, 0, 14 (z = 4.11); −4, −4, 12 (z = 4.07); FWE p < 0.05 SVC
        Cerebellum20, −52, −24 (z = 5.10)
        Dorsomedial prefrontal cortex12, 64, 26 (z = 4.24)
        Anterior cingulate cortex−4, 36, 28 (z = 3.45)
    Choice kernelp < 0.001 (uncorrected)
        Nucleus accumbens−4, 10, −8 (z = 4.29)
        Dosomedial prefrontal cortex−6, 60, 34 (z = 4.32)
        Ventromedial prefrontal cortex−12, 44, −4 (z = 3.88)
    Choice kernal x -serotonin (ΔTRP:ΣLNAA)p < 0.001 (uncorrected)
        Right head of caudate18, 4, 14 (z = 4.91); FWE p < 0.05 (whole brain)
        Anterior cingulate cortex−2, 42, 16 (z = 3.32)
        Anterior pole16, 66, 10 (z = 3.37)*
    Avoidance prediction errorp < 0.001 (uncorrected)
        Right head of caudate12, 2, 18 (z = 4.08); FWE p < 0.05 SVC
        Bilateral dorsolateral putamen30, 0, 8 (z = 3.76); −22, 0, 8 (z = 3.53); FWE p < 0.05 SVC
        Ventrolateral putamen30, −8, −6 (z = 4.63)
        Bilateral amygdaloid complex24, 2, −12 (z = 3.84); −28, −4, −14 (z = 3.54)
    Overlapping reward and avoidance prediction errorp < 0.01 × p < 0.01 (uncorrected)
        Right head of caudate10, 12, 6
        Right dorsolateral putamen28, 0, 6
    Reward prediction error × serotonin (ΔTRP:ΣLNAA)p < 0.001 (uncorrected); FWE p < 0.05 SVC
        Right dorsolateral putamen34, −4, 4 (z = 4.22)
    • Results in bold are a priori ROIs (ventromedial PFC, choice values; dorsal striatum, instrumental prediction errors; see Materials and Methods). SVC, Small volume correction.

    • ↵*Not SVC as distinct from previous anterior pole activity related to exploration.

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The Journal of Neuroscience: 32 (17)
Journal of Neuroscience
Vol. 32, Issue 17
25 Apr 2012
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Serotonin Selectively Modulates Reward Value in Human Decision-Making
Ben Seymour, Nathaniel D. Daw, Jonathan P. Roiser, Peter Dayan, Ray Dolan
Journal of Neuroscience 25 April 2012, 32 (17) 5833-5842; DOI: 10.1523/JNEUROSCI.0053-12.2012

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Serotonin Selectively Modulates Reward Value in Human Decision-Making
Ben Seymour, Nathaniel D. Daw, Jonathan P. Roiser, Peter Dayan, Ray Dolan
Journal of Neuroscience 25 April 2012, 32 (17) 5833-5842; DOI: 10.1523/JNEUROSCI.0053-12.2012
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