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Cognitive Models as a Tool to Link Decision Behavior with EEG Signals

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An Introduction to Model-Based Cognitive Neuroscience

Abstract

EEG is a direct measure of cortical neuronal activities, making it particularly well-suited to identify latent computations that underlie learning and decision making. This chapter takes a targeted look at how EEG signals and cognitive models of decision making can be linked in a mutually beneficial way. The first section begins with a tutorial on commonly used “linking” approaches, with a focus on sequential sampling models of decision making. This includes a depiction of increasingly sophisticated studies: from condition-level summaries of EEG signals with independently estimated model parameters to regressing trial-level EEG signals with trial-level estimates of model parameters. We then draw attention to joint modeling approaches that assess the bidirectional relationship between EEG signals and parameters of cognitive models. These approaches provide integrated, confirmatory frameworks that propose a common latent source that generates predictions for multiple outputs, such as behavior and neural data. The second section is a review of linking approaches in reinforcement learning models of decision making. This includes a brief history of formal linking approaches between EEG and reinforcement learning, from origins in qualitative comparison of prediction errors and aggregate EEG summaries through to regression of individual-trial data. The chapter concludes with some caveats to current linking approaches and a discussion of potential future directions for advancing the methods of linking EEG signals with cognitive models.

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Notes

  1. 1.

    To simplify the tutorial, Eq. 1 is a simplified form of the model examined in Cavanagh et al. (2011). We refer the reader to the primary source for the complete model.

  2. 2.

    Van Ravenzwaaij et al. (2017) tested multiple joint models with different linking functions. For brevity, we describe just one of those models.

References

  • Brown, D. R., & Cavanagh, J. F. (2018). Rewarding images do not invoke the reward positivity: They inflate it. International Journal of Psychophysiology, 132, 226–235.

    Article  PubMed  PubMed Central  Google Scholar 

  • Calhoun, V. D., Liu, J., & Adalı, T. (2009). A review of group ICA for FMRI data and ICA for joint inference of imaging, genetic, and ERP data. NeuroImage, 45(1), S163–S172.

    Article  PubMed  Google Scholar 

  • Caplin, A., & Dean, M. (2008). Axiomatic methods, dopamine and reward prediction error. Current Opinion in Neurobiology, 18(2), 197–202.

    Article  PubMed  Google Scholar 

  • Cassey, P. J., Gaut, G., Steyvers, M., & Brown, S. D. (2016) A generative joint model for spike trains and saccades during perceptual decision-making. Psychonomic Bulletin & Review, 23(6):1757–1778

    Article  Google Scholar 

  • Cavanagh, J. F. (2015). Cortical delta activity reflects reward prediction error and related behavioral adjustments, but at different times. NeuroImage, 110, 205–216.

    Article  PubMed  Google Scholar 

  • Cavanagh, J. F. (2019). Electrophysiology as a theoretical and methodological hub for the neural sciences. Psychophysiology, 56(2), e13314.

    Article  PubMed  Google Scholar 

  • Cavanagh, J. F., Bismark, A. W., Frank, M. J., & Allen, J. J. (2019a). Multiple dissociations between comorbid depression and anxiety on reward and punishment processing: Evidence from computationally informed EEG. Computational Psychiatry, 3, 1–17.

    Article  PubMed  Google Scholar 

  • Cavanagh, J. F., Eisenberg, I., Guitart-Masip, M., Huys, Q., & Frank, M. J. (2013). Frontal theta overrides Pavlovian learning biases. Journal of Neuroscience, 33(19), 8541–8548.

    Article  PubMed  Google Scholar 

  • Cavanagh, J. F., & Frank, M. J. (2014). Frontal theta as a mechanism for cognitive control. Trends in Cognitive Sciences, 18(8), 414–421.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cavanagh, J. F., Figueroa, C. M., Cohen, M. X., & Frank, M. J. (2012a). Frontal theta reflects uncertainty and unexpectedness during exploration and exploitation. Cerebral Cortex, 22(11), 2575–2586.

    Article  PubMed  Google Scholar 

  • Cavanagh, J. F., Frank, M. J., Klein, T. J., & Allen, J. J. (2010). Frontal theta links prediction errors to behavioral adaptation in reinforcement learning. Neuroimage, 49(4), 3198–3209.

    Article  PubMed  Google Scholar 

  • Cavanagh, J. F., Kumar, P., Mueller, A. A., Richardson, S. P., & Mueen, A. (2018). Diminished EEG habituation to novel events effectively classifies Parkinson’s patients. Clinical Neurophysiology, 129(2), 409–418.

    Article  PubMed  Google Scholar 

  • Cavanagh, J. F., Rieger, R. E., Wilson, J. K., Gill, D., Fullerton, L., Brandt, E., & Mayer, A. R. (2019b). Joint analysis of frontal theta synchrony and white matter following mild traumatic brain injury. Brain Imaging and Behavior, 14(6), 2210–2223

    Article  Google Scholar 

  • Cavanagh, J. F., Wiecki, T. V., Cohen, M. X., Figueroa, C. M., Samanta, J., Sherman, S. J., & Frank, M. J. (2011). Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold. Nature Neuroscience, 14, 1462–1467.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cavanagh, J. F., Zambrano-Vazquez, L., & Allen, J. J. (2012b). Theta lingua franca: A common mid-frontal substrate for action monitoring processes. Psychophysiology, 49(2), 220–238.

    Article  PubMed  Google Scholar 

  • Chase, H. W., Swainson, R., Durham, L., Benham, L., & Cools, R. (2011). Feedback-related negativity codes prediction error but not behavioral adjustment during probabilistic reversal learning. Journal of Cognitive Neuroscience, 23(4), 936–946.

    Article  PubMed  Google Scholar 

  • Cockburn, J., & Holroyd, C. B. (2018). Feedback information and the reward positivity. International Journal of Psychophysiology, 132, 243–251.

    Article  PubMed  Google Scholar 

  • Cohen, M. X. (2014). Analyzing neural time series data: Theory and practice. MIT Press.

    Book  Google Scholar 

  • Cohen, M. X. (2018). Using spatiotemporal source separation to identify prominent features in multichannel data without sinusoidal filters. European Journal of Neuroscience, 48(7), 2454–2465.

    Article  PubMed  Google Scholar 

  • Cohen, M. X., & Donner, T. H. (2013). Midfrontal conflict-related theta-band power reflects neural oscillations that predict behavior. Journal of Neurophysiology, 110(12), 2752–2763.

    Article  PubMed  Google Scholar 

  • Cohen, M. X., & Ranganath, C. (2007). Reinforcement learning signals predict future decisions. Journal of Neuroscience, 27(2), 371–378.

    Article  PubMed  Google Scholar 

  • Collins, A. G. E., & Frank, M. J. (2012). How much of reinforcement learning is working memory, not reinforcement learning? A behavioral, computational, and neurogenetic analysis. European Journal of Neuroscience, 35(7), 1024–1035.

    Article  PubMed  Google Scholar 

  • Collins, A. G. E., & Frank, M. J. (2016). Neural signature of hierarchically structured expectations predicts clustering and transfer of rule sets in reinforcement learning. Cognition, 152, 160–169.

    Article  PubMed  PubMed Central  Google Scholar 

  • Collins, A. G. E., & Frank, M. J. (2018). Within-and across-trial dynamics of human eeg reveal cooperative interplay between reinforcement learning and working memory. Proceedings of the National Academy of Sciences, 115(10), 2502–2507.

    Article  Google Scholar 

  • Collins, A. G. E., & Koechlin, E. (2012). Reasoning, learning, and creativity: Frontal lobe function and human decision-making. PLoS Biology, 10(3), e1001293.

    Article  PubMed  PubMed Central  Google Scholar 

  • Correa, C. M., Noorman, S., Jiang, J., Palminteri, S., Cohen, M. X., Lebreton M, & van Gaal S. (2018). How the level of reward awareness changes the computational and electrophysiological signatures of reinforcement learning. Journal of Neuroscience, 38(48), 10338–10348.

    Article  PubMed  Google Scholar 

  • Dien, J. (2012). Applying principal components analysis to event-related potentials: A tutorial. Developmental Neuropsychology, 37(6), 497–517.

    Article  PubMed  Google Scholar 

  • Dien, J., Khoe, W., & Mangun, G. R. (2007). Evaluation of PCA and ICA of simulated ERPS: Promax vs. Infomax rotations. Human Brain Mapping, 28(8),742–763.

    Article  PubMed  Google Scholar 

  • Eppinger, B., Walter, M., & Li, S. C. (2017). Electrophysiological correlates reflect the integration of model-based and model-free decision information. Cognitive, Affective, & Behavioral Neuroscience, 17(2), 406–421.

    Article  Google Scholar 

  • Fischer, A. G., & Ullsperger, M. (2013). Real and fictive outcomes are processed differently but converge on a common adaptive mechanism. Neuron, 79(6), 1243–1255.

    Article  PubMed  Google Scholar 

  • Folstein, J. R., & Van Petten, C. (2008). Influence of cognitive control and mismatch on the n2 component of the ERP: A review. Psychophysiology, 45(1), 152–170.

    Article  PubMed  Google Scholar 

  • Forstmann, B. U., Dutilh, G., Brown, S., Neumann, J., Von Cramon, D. Y., Ridderinkhof, K. R., & Wagenmakers, E. J. (2008). Striatum and pre-SMA facilitate decision-making under time pressure. Proceedings of the National Academy of Sciences, 105(45), 17538–17542.

    Article  Google Scholar 

  • Frank, M. J. (2005). Dynamic dopamine modulation in the basal ganglia: A neurocomputational account of cognitive deficits in medicated and nonmedicated parkinsonism. Journal of Cognitive Neuroscience, 17(1), 51–72.

    Article  PubMed  Google Scholar 

  • Fries, P. (2009). Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annual Review of Neuroscience, 32, 209–224.

    Article  PubMed  Google Scholar 

  • Friston, K. (2003). Learning and inference in the brain. Neural Networks, 16(9), 1325–1352.

    Article  PubMed  Google Scholar 

  • Friston, K. (2005). A theory of cortical responses. Philosophical Transactions of the Royal Society B: Biological Sciences, 360(1456), 815–836.

    Article  Google Scholar 

  • Friston, K. (2010). The free-energy principle: A unified brain theory? Nature Reviews Neuroscience, 11(2), 127–138.

    Article  PubMed  Google Scholar 

  • Hauser, T. U., Iannaccone, R., Stämpfli, P., Drechsler, R., Brandeis, D., Walitza, S., & Brem, S. (2014). The feedback-related negativity (FRN) revisited: New insights into the localization, meaning and network organization. NeuroImage, 84, 159–168.

    Article  PubMed  Google Scholar 

  • Holroyd, C. B., & Coles, M. G. (2002). The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychological Review, 109(4), 679.

    Article  PubMed  Google Scholar 

  • Holroyd, C. B., Pakzad-Vaezi, K. L., & Krigolson, O. E. (2008). The feedback correct-related positivity: Sensitivity of the event-related brain potential to unexpected positive feedback. Psychophysiology, 45(5), 688–697.

    Article  PubMed  Google Scholar 

  • Hunt, L. T., Kolling, N., Soltani, A., Woolrich, M. W., Rushworth, M. F. S., & Behrens, T. E. J. (2012). Mechanisms underlying cortical activity during value-guided choice. Nature Neuroscience, 15(3), 470–476.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ichikawa, N., Siegle, G. J., Dombrovski, A., & Ohira, H. (2010). Subjective and model-estimated reward prediction: Association with the feedback-related negativity (FRN) and reward prediction error in a reinforcement learning task. International Journal of Psychophysiology, 78(3), 273–283.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karayanidis, F., Mansfield, E. L., Galloway, K. L., Smith, J. L., Provost, A., & Heathcote, A. J. (2009). Anticipatory reconfiguration elicited by fully and partially informative cues that validly predict a switch in task. Cognitive, Affective, & Behavioral Neuroscience, 9, 202–215.

    Article  Google Scholar 

  • Luck, S. J. (2014). An introduction to the event-related potential technique. MIT Press.

    Google Scholar 

  • Ly, A., Boehm, U., Heathcote, A., Turner, B. M., Forstmann, B. U., Marsman, M., & Matzke, D. (2018). A flexible and efficient hierarchical Bayesian approach to the exploration of individual differences in cognitive-model-based neuroscience. In A. A. Moustafa (Ed.), Computational models of brain and behavior. Wiley Blackwell.

    Google Scholar 

  • Nassar, M. R., Bruckner, R., & Frank, M. J. (2019). Statistical context dictates the relationship between feedback-related EEG signals and learning. Elife, 8, e46975.

    Article  PubMed  PubMed Central  Google Scholar 

  • Otto, A. R., Skatova, A., Madlon-Kay, S., & Daw, N. D. (2014). Cognitive control predicts use of model-based reinforcement learning. Journal of Cognitive Neuroscience, 27(2), 319–333.

    Article  Google Scholar 

  • Pedersen, M. L., Frank, M. J., & Biele, G. (2017). The drift diffusion model as the choice rule in reinforcement learning. Psychonomic Bulletin & Review, 24(4), 1234–1251.

    Article  Google Scholar 

  • Pessoa, L. (2008). On the relationship between emotion and cognition. Nature Reviews Neuroscience, 9(2), 148–158.

    Article  PubMed  Google Scholar 

  • Philiastides, M. G., Biele, G., Vavatzanidis, N., Kazzer, P., & Heekeren, H. R. (2010). Temporal dynamics of prediction error processing during reward-based decision making. NeuroImage, 53(1), 221–232.

    Article  PubMed  Google Scholar 

  • Proudfit, G. H. (2015). The reward positivity: From basic research on reward to a biomarker for depression. Psychophysiology, 52(4), 449–459.

    Article  PubMed  Google Scholar 

  • Provost, A., Johnson, B., Karayanidis, F., Brown, S. D., & Heathcote, A. (2013). Two routes to expertise in mental rotation. Cognitive Science, 37(7), 1321–1342.

    Article  PubMed  Google Scholar 

  • Rac-Lubashevsky, R., & Kessler, Y. (2019). Revisiting the relationship between the p3b and working memory updating. Biological Psychology, 148, 107769.

    Article  PubMed  Google Scholar 

  • Rescorla, R., & Wagner, A. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In A. Black, & W. Prokasy (Eds.), Classical conditioning II: Current research and theory (pp. 64–99). Appleton-Century Crofts.

    Google Scholar 

  • Ribas-Fernandes, J. J., Solway, A., Diuk, C., McGuire, J. T., Barto, A. G., Niv, Y., & Botvinick, M. M. (2011). A neural signature of hierarchical reinforcement learning. Neuron, 71(2), 370–379.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rouder, J. N., & Haaf, J. M. (2019). A psychometrics of individual differences in experimental tasks. Psychonomic Bulletin & Review, 26(2), 452–467.

    Article  Google Scholar 

  • Sambrook, T. D., & Goslin, J. (2014). Mediofrontal event-related potentials in response to positive, negative and unsigned prediction errors. Neuropsychologia, 61, 1–10.

    Article  PubMed  Google Scholar 

  • Sambrook, T. D., Hardwick, B., Wills, A. J., & Goslin, J. (2018). Model-free and model-based reward prediction errors in EEG. NeuroImage, 178, 162–171.

    Article  PubMed  Google Scholar 

  • Schultz, W., Dayan, P., & Montague, P. R. (1997). A neural substrate of prediction and reward. Science, 275, 1593–1599.

    Article  PubMed  Google Scholar 

  • Shackman, A. J., Salomons, T. V., Slagter, H. A., Fox, A. S., Winter, J. J., & Davidson, R. J. (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Reviews Neuroscience, 12(3), 154–167.

    Article  PubMed  PubMed Central  Google Scholar 

  • Siegel, M., Donner, T. H., & Engel, A. K. (2012). Spectral fingerprints of large-scale neuronal interactions. Nature Reviews Neuroscience, 13(2), 121–134.

    Article  PubMed  Google Scholar 

  • Sutton, R. S., & Barto, A. G. (1998). Reinforcement Learning: An Introduction. MIT Press.

    Google Scholar 

  • Talmi, D., Atkinson, R., & El-Deredy, W. (2013). The feedback-related negativity signals salience prediction errors, not reward prediction errors. Journal of Neuroscience, 33(19):8264–8269.

    Article  PubMed  Google Scholar 

  • Thorndike, E. (1898). Animal intelligence: An experimental study of the associative processes in animals. The Psychological Review: Monograph Supplements, 2(4), i–109.

    Google Scholar 

  • Threadgill, A. H., & Gable, P. A. (2018). The sweetness of successful goal pursuit: Approach-motivated pregoal states enhance the reward positivity during goal pursuit. International Journal of Psychophysiology, 132, 277–286.

    Article  PubMed  Google Scholar 

  • Turner, B. M., Forstmann, B. U., Love, B. C., Palmeri, T. J., & Van Maanen, L. (2017). Approaches to analysis in model-based cognitive neuroscience. Journal of Mathematical Psychology, 76, 65–79.

    Article  PubMed  Google Scholar 

  • Turner, B. M., Forstmann, B. U., & Steyvers, M. (2019). Joint models of neural and behavioral data. Springer.

    Book  Google Scholar 

  • Van Ravenzwaaij, D., Provost, A., & Brown, S. D. (2017). A confirmatory approach for integrating neural and behavioral data into a single model. Journal of Mathematical Psychology, 76, 131–141.

    Article  Google Scholar 

  • Wagenmakers, E. J., van der Maas, H. J. L., Dolan, C., & Grasman, R. P. P. P. (2008). Ez does it! Extensions of the EZ-diffusion model. Psychonomic Bulletin & Review, 15, 1229–1235.

    Article  Google Scholar 

  • Whitton, A. E., Kakani, P., Foti, D., Van’t Veer, A., Haile, A., Crowley, D. J., & Pizzagalli, D. A. (2016) Blunted neural responses to reward in remitted major depression: A high-density event-related potential study. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 1(1), 87–95.

    PubMed  Google Scholar 

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Acknowledgements

Funding This work was supported by: Australian Research Council (ARC) Discovery Early Career Researcher Award (Hawkins, DE170100177); ARC Discovery Project (Hawkins and Brown, DP180103613); National Institutes of Mental Health (Cavanagh, NIMH RO1MH119382-01). The funding sources had no role in the study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

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Correspondence to Guy E. Hawkins .

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Hawkins, G.E., Cavanagh, J.F., Brown, S.D., Steyvers, M. (2024). Cognitive Models as a Tool to Link Decision Behavior with EEG Signals. In: Forstmann, B.U., Turner, B.M. (eds) An Introduction to Model-Based Cognitive Neuroscience. Springer, Cham. https://doi.org/10.1007/978-3-031-45271-0_10

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