A multivariate brain signature for reward

Poster No:

1598 

Submission Type:

Abstract Submission 

Authors:

Judit Campdepadrós Barrios1, Sebastian Speer2, Christian Keysers3, Cas Teurlings3, Ale Smidts4, Maarten Boksem4, Tor Wager5, Valeria Gazzola3

Institutions:

1Netherlands Institute for Neuroscience, Amsterdam, NH, 2Princeton Neuroscience Institute, Princeton, NJ, 3Netherlands Institute for Neuroscience, Amsterdam, North Holland, 4Rotterdam School of Management, Rotterdam, South Holland, 5Department of Psychological and Brain Sciences, Hanover, NH

First Author:

Judit Campdepadrós Barrios  
Netherlands Institute for Neuroscience
Amsterdam, NH

Co-Author(s):

Sebastian Speer  
Princeton Neuroscience Institute
Princeton, NJ
Christian Keysers  
Netherlands Institute for Neuroscience
Amsterdam, North Holland
Cas Teurlings  
Netherlands Institute for Neuroscience
Amsterdam, North Holland
Ale Smidts  
Rotterdam School of Management
Rotterdam, South Holland
Maarten Boksem  
Rotterdam School of Management
Rotterdam, South Holland
Tor Wager  
Department of Psychological and Brain Sciences
Hanover, NH
Valeria Gazzola  
Netherlands Institute for Neuroscience
Amsterdam, North Holland

Introduction:

Reward and punishment processing is vital for adaptive behavior, with its dysregulation implicated in mental health and substance use disorders. Traditional univariate approaches to reward processing often yield small effect sizes and limited reliability. In contrast, multivariate methods decode distributed neural patterns, providing higher sensitivity and specificity (Reddan et al. 2017). In this study (Speer et al. 2023), we developed the Brain Reward Signature (BRS), a multivariate brain model (Kragel et al. 2018) to predict the magnitude of rewards and losses in decision-making tasks.

Methods:

The BRS was trained using data from five fMRI tasks across four independent samples (N = 1169). Initially, we trained a LASSO-PCR model on data from a Monetary Incentive Delay (MIDtrain) task (N = 39), predicting three levels of monetary reward. We selected voxels correlating more strongly with outcomes than salience to ensure specificity and used 5-fold cross-validation to prevent overfitting. The study used out-of-sample prediction to assess the brain regions' contributions to predicting monetary outcomes (Fig. 1A), with prediction accuracy evaluated using Spearman correlation at each fold. The resulting pattern maps were thresholded at p<0.001 through bootstrap analysis in the MIDtrain dataset (Fig. 1B). Validation tests included another MID task (MIDval; N = 12: Srirangarajan et al. 2021), a Gambling task (HCP, N = 1084: Van Essen et al., 2012), a Disgust-Delay Task (DDT, N = 39), and an Emotion Viewing Task (EVT, N = 27: manuscript in preparation).
Supporting Image: Fig1.png
 

Results:

The BRS successfully predicted outcomes in unseen subjects (RMSE = 2.89, r = 0.72, pperm < 0.001, BF10 > 1000) and achieved 92% accuracy in decoding rewards versus losses (Fig. 2A). It generalized to a different MID version and sample (RMSE = 2.97, r = 0.75, pperm < 0.001, BF10 > 1000), with 92% forced-choice accuracy in decoding high reward versus high loss (Fig. 2B). It also predicted outcomes in a gambling task (r = 0.21, pperm < 0.001, BF10 > 100), achieving 73% forced-choice accuracy in distinguishing high reward versus high loss (Fig. 2C). The BRS also predicted non-financial reinforcers in the DDT (r = 0.38, pperm < 0.001, BF10 > 100), by discriminating successful from unsuccessful trials in the feedback phase with 92% accuracy (Fig. 2E). However, it did not generalize to emotional salient outcomes, failing to distinguish between disgusting and neutral images (r = -0.13, pperm < 0.28, BF10 = 0.23; Fig. 2D). In the EVT, BRS values were positive across both positive and negative emotional facial expressions (all t > 4.5, p <0.001, BF10 > 100; Fig. 2F), suggesting it may capture processes like morbid curiosity. Supporting this hypothesis, an online sample (N = 200) rated high-intensity emotional videos (happy, angry, fearful, painful, and disgusting) as more interesting than neutral ones (all p < 0.001, all BF10 > 46). In addition, the BRS has already been applied successfully in a moral conflict learning task, loading positively on prediction errors for both money (receiving higher than expected monetary rewards) and painful shocks to another individual (for less intense than expected shocks; Fornari et al., 2023).
Supporting Image: Fig2.png
 

Conclusions:

The BRS robustly decodes the magnitude of reward and losses across tasks, generalizing to different samples and non-financial reinforcers, namely positive feedback and avoiding pain. Crucially, its specificity to rewarding outcomes, without extending to choice-dependent disgust outcomes, aligns with its intended purpose of capturing reward-related processes rather than unrelated affective responses. Additionally, its positive loading on non-action-contingent outcomes suggests sensitivity to broader processes, such as morbid curiosity (Oosterwijk et al., 2020). These findings underscore the utility and reliability of the BRS within its intended scope, while recognizing that any signature can be further refined and validated by testing across more diverse datasets.

Emotion, Motivation and Social Neuroscience:

Reward and Punishment 2

Modeling and Analysis Methods:

Multivariate Approaches 1

Keywords:

MRI
Multivariate
Other - reward, loss, neural signature, decoding, machine learning

1|2Indicates the priority used for review

Abstract Information

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Were any human subjects research approved by the relevant Institutional Review Board or ethics panel? NOTE: Any human subjects studies without IRB approval will be automatically rejected.

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Functional MRI
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Other, Please list  -   fMRIPrep version 1.0.8

Provide references using APA citation style.

Fornari, L., Ioumpa, K., Nostro, A. D., Evans, N. J., De Angelis, L., Speer, S. P. H., Paracampo, R., Gallo, S., Spezio, M., Keysers, C., & Gazzola, V. (2023). Neuro-computational mechanisms and individual biases in action-outcome learning under moral conflict. Nature communications, 14(1), 1218. https://doi.org/10.1038/s41467-023-36807-3

Kragel, P. A., Koban, L., Barrett, L. F., & Wager, T. D. (2018). Representation, pattern information, and brain signatures: From neurons to neuroimaging. Neuron, 99(2), 257–273. https://doi.org/10.1016/j.neuron.2018.06.009

Oosterwijk, S., Snoek, L., Tekoppele, J. et al. Choosing to view morbid information involves reward circuitry. Sci Rep 10, 15291 (2020). https://doi.org/10.1038/s41598-020-71662-y

Reddan, M. C., Lindquist, M. A., & Wager, T. D. (2017). Effect size estimation in neuroimaging. JAMA Psychiatry, 74(3), 207–208. https://doi.org/10.1001/jamapsychiatry.2016.3356

Speer, S. P. H., Keysers, C., Campdepadrós Barrios, J., Teurlings, C. J. S., Smidts, A., Boksem, M. A. S., Wager, T. D., & Gazzola, V. (2023). A multivariate brain signature for reward. NeuroImage, 119990. https://doi.org/10.1016/j.neuroimage.2023.119990

Srirangarajan, T., Mortazavi, L., Bortolini, T., Moll, J., & Knutson, B. (2021). Multi‐band fMRI compromises detection of mesolimbic reward responses. NeuroImage, 237, 118617. https://doi.org/10.1016/j.neuroimage.2021.118617

Van Essen, D. C., Ugurbil, K., Auerbach, E., Barch, D., Behrens, T. E. J., Bucholz, R., Chang, A., Chen, L., Corbetta, M., Curtiss, S. W., Della Penna, S., Feinberg, D., Glasser, M. F., Harel, N., Heath, A. C., Larson-Prior, L., Marcus, D., Michalareas, G., Moeller, S., Oostenveld, R., Yacoub, E. (2012). The Human Connectome Project: A data acquisition perspective. NeuroImage, 62(4), 2222–2231. https://doi.org/10.1016/j.neuroimage.2012.02.018

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