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Articles, Behavioral/Cognitive

fMRI and EEG Predictors of Dynamic Decision Parameters during Human Reinforcement Learning

Michael J. Frank, Chris Gagne, Erika Nyhus, Sean Masters, Thomas V. Wiecki, James F. Cavanagh and David Badre
Journal of Neuroscience 14 January 2015, 35 (2) 485-494; https://doi.org/10.1523/JNEUROSCI.2036-14.2015
Michael J. Frank
1Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
2Brown Institute for Brain Science, Providence, Rhode Island 09212,
3Department of Psychiatry and Human Behavior, Brown University, Providence, Rhode Island 02912,
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Chris Gagne
1Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
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Erika Nyhus
1Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
4Department of Psychology and Program in Neuroscience, Bowdoin College, Brunswick, Maine 04011, and
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Sean Masters
1Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
2Brown Institute for Brain Science, Providence, Rhode Island 09212,
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Thomas V. Wiecki
1Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
2Brown Institute for Brain Science, Providence, Rhode Island 09212,
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James F. Cavanagh
1Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
5Department of Psychology, University of New Mexico, Albuquerque, New Mexico 87131
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David Badre
1Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island 02912,
2Brown Institute for Brain Science, Providence, Rhode Island 09212,
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    Figure 1.

    Probabilistic reinforcement learning task. A, Task/trial structure. Participants learned to select one of two motor responses for three different stimuli with different reward contingencies (85:15, 75:25, and 65:35% reward probabilities). B, Evolution of model-estimated action values as a function of experience, from an example subject and condition (p(r|a) = 0.35 and 0.65). The difference in values at each point in time was used as a regressor onto the drift rate in the DDM. Conflict is high on trials in which the values of the two choice options is similar. C, Mean evolution of the difference in model-estimated action values for each condition across all subjects, based on each subject's choice and reinforcement history. D, Mean behavioral learning curves in these conditions across subjects.

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    Figure 2.

    Choice proportions and RT distributions are captured by RL-DDM. A, Behavioral RT distributions across the group are shown for each reward condition (red, smoothed with kernel density estimation), together with posterior predictive simulations from the RL-DDM (blue). Distributions to the right correspond to choices of the high-valued option and those to the left represent choices of the low-valued option. The relative area under each distribution defines the choice proportions (i.e., greater area to the right than left indicates higher proportion choices of the more rewarding action). Accuracy is worse, and tails of the distribution are longer, with lower reward probability. B, Model fit to behavior can be more precisely viewed using a quantile-probability plot, showing choices and quantiles of RT distributions. Choice probability is plotted along the x-axis separately for choices involving low, medium, and high differences in values (tertiles of value differences assessed by the RL model). Values on the x-axis >0.5 indicate proportion of choices of the high-valued option, and those <0.5 indicate choice proportions of the low-valued option, each with their corresponding RT quantiles on the y-axis. For example, when value differences were medium, subjects chose the high-valued option ∼80% of the time, and the first RT quantile of that choice occurred at ∼475 ms. Empirical behavioral choices/RT quantiles are marked as X and simulated RTs from the posterior predictive of the RL-DDM as ellipses (capturing uncertainty). Quantiles are computed for each subject separately and then averaged to yield group quantiles. Ellipse widths represent SD of the posterior predictive distribution from the model and indicate estimation uncertainty.

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    Figure 3.

    Graphical model showing hierarchical estimation of RL-DDM with trial-wise neural regressors. Round nodes represent continuous random variables, and double- bordered nodes represent deterministic variables, defined in terms of other variables. Shaded nodes represent observed data, including trial-wise behavioral data (accuracy, RT) and neural measures (fMRI and EEG). Open nodes represent unobserved latent parameters. Overall subject-wise parameters are estimated from individuals drawn from a group distribution with inferred mean μ and variance σ. Trial-wise variations of decision threshold a and drift rate v (residuals from the subject-wise values) are determined by neural measures and latent RL value difference/conflict. Plates denote that multiple random variables share the same parents and children (e.g., each subject-wise threshold parameter aS shares the same parents that define the group distribution). The outer plate is over subjects S while the inner plate is over trials T. Inferred relationships of trial-wise regressors were estimated as fixed effect across the group, as regularization and to prevent parameter explosion. sv = SD of drift rate across trials; t = time for encoding and response execution (“nondecision time”).

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    Figure 4.

    Combining fMRI and EEG to estimate DM parameters. A, Trial-to-trial peak estimates of the BOLD signal from pre-SMA and STN ROIs (depicted on sagittal slices) along with trial-to-trial theta power estimates from mid-frontal EEG, were entered in as regressors to DDM parameters. The upper response boundary represents choices of the high-valued option, whereas the lower response boundary represents choices of the suboptimal option. Decision threshold reflects the distance between the boundaries, and the drift rate (speed of evidence accumulation) is proportional to the value difference between options. B, Posterior distributions on model parameter estimates, showing estimated regression coefficients whereby drift rate was found to be proportional to value differences and decision threshold proportional to various markers of neural activity and their interaction with decision conflict. Peak values of each distribution represent the best estimates of each parameter, and the width of the distribution represents its uncertainty. Drift rate was significantly related to the (dynamically varying across trials) value difference between each option (posterior distribution shifted far to the right of zero). Decision threshold was significantly related to STN BOLD; the interaction between pre-SMA BOLD and conflict; and the three-way interaction between mid-frontal theta power, STN BOLD, and conflict.

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    Figure 5.

    EEG and fMRI correlates of decision conflict. A, Mid-frontal theta power from EEG locked to stimulus onset, showing a strong increase in theta power across all subjects and trials. B, Trial-to-trial correlation between mid-frontal theta power from EEG and BOLD activity, showing strongest correlation in the SMA. Activation shown is thresholded at p < 0.001 uncorrected with a clustering extent of 120 voxels (corrected p value of p < 0.046 FWE). C, PPI identifies brain regions that preferentially respond as both mPFC theta and conflict rise, showing an isolated cluster of subcortical voxels overlapping with STN mask.

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The Journal of Neuroscience: 35 (2)
Journal of Neuroscience
Vol. 35, Issue 2
14 Jan 2015
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fMRI and EEG Predictors of Dynamic Decision Parameters during Human Reinforcement Learning
Michael J. Frank, Chris Gagne, Erika Nyhus, Sean Masters, Thomas V. Wiecki, James F. Cavanagh, David Badre
Journal of Neuroscience 14 January 2015, 35 (2) 485-494; DOI: 10.1523/JNEUROSCI.2036-14.2015

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fMRI and EEG Predictors of Dynamic Decision Parameters during Human Reinforcement Learning
Michael J. Frank, Chris Gagne, Erika Nyhus, Sean Masters, Thomas V. Wiecki, James F. Cavanagh, David Badre
Journal of Neuroscience 14 January 2015, 35 (2) 485-494; DOI: 10.1523/JNEUROSCI.2036-14.2015
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Keywords

  • basal ganglia
  • decision making
  • drift diffusion model
  • prefrontal cortex
  • subthalamic nucleus

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