Neural surprise in somatosensory Bayesian learning

Sam Gijsen, Miro Grundei, Robert T Lange, Dirk Ostwald and Felix Blankenburg

PLOS Computational Biology, 2021, vol. 17, issue 2, 1-36

Abstract: Tracking statistical regularities of the environment is important for shaping human behavior and perception. Evidence suggests that the brain learns environmental dependencies using Bayesian principles. However, much remains unknown about the employed algorithms, for somesthesis in particular. Here, we describe the cortical dynamics of the somatosensory learning system to investigate both the form of the generative model as well as its neural surprise signatures. Specifically, we recorded EEG data from 40 participants subjected to a somatosensory roving-stimulus paradigm and performed single-trial modeling across peri-stimulus time in both sensor and source space. Our Bayesian model selection procedure indicates that evoked potentials are best described by a non-hierarchical learning model that tracks transitions between observations using leaky integration. From around 70ms post-stimulus onset, secondary somatosensory cortices are found to represent confidence-corrected surprise as a measure of model inadequacy. Indications of Bayesian surprise encoding, reflecting model updating, are found in primary somatosensory cortex from around 140ms. This dissociation is compatible with the idea that early surprise signals may control subsequent model update rates. In sum, our findings support the hypothesis that early somatosensory processing reflects Bayesian perceptual learning and contribute to an understanding of its precise mechanisms.Author summary: Our environment features statistical regularities, such as a drop of rain predicting imminent rainfall. Despite the importance for behavior and survival, much remains unknown about how these dependencies are learned, particularly for somatosensation. As surprise signalling about novel observations indicates a mismatch between one’s beliefs and the world, it has been hypothesized that surprise computation plays an important role in perceptual learning. By analyzing EEG data from human participants receiving sequences of tactile stimulation, we compare different formulations of surprise and investigate the employed underlying learning model. Our results indicate that the brain estimates transitions between observations. Furthermore, we identified different signatures of surprise computation and thereby provide a dissociation of the neural correlates of belief inadequacy and belief updating. Specifically, early surprise responses from around 70ms were found to signal the need for changes to the model, with encoding of its subsequent updating occurring from around 140ms. These results provide insights into how somatosensory surprise signals may contribute to the learning of environmental statistics.

Date: 2021
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pcbi00:1008068

DOI: 10.1371/journal.pcbi.1008068

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