The cost of scrutiny: subclinical social anxiety and performance context reshape frontal-midline theta network reconfigurations during probabilistic learning

Social anxiety is reliably characterized by biases toward avoidance and aversive learning. Frontal-midline theta (FM-theta) oscillations have been implicated as a key neural mechanism underlying these learning biases. Here we combined a dynamic network neuroscience approach with computational modeling to investigate how FM-theta oscillatory activity coordinates large-scale functional network interactions on a trial-to-trial basis during feedback-guided learning. Additionally, we examined how these neural dynamics are altered in social anxiety across different social contexts. A sample of 146 human participants (129 female, mean age = 20.4 years) with varying levels of social anxiety completed a probabilistic selection task while performing alone and under scrutiny. Using non-negative matrix factorization, we identified two functional neural subgraphs supported by FM-theta. Fronto-parietal connectivity increased following aversive outcomes and scaled with positive prediction errors, consistent with error-monitoring and belief-updating. Fronto-occipital connectivity scaled with prediction errors when performing alone but not under scrutiny, indicative of context-sensitive disruption of belief-updating. Participants with elevated social anxiety showed increased fronto-occipital connectivity, as well as stronger subgraph coupling, indexing cross-network integration. This latter effect facilitated learning of simple stimulus-reward associations, but hampered learning of difficult stimulus-reward associations. Together, these findings reveal that social anxiety amplifies fronto-occipital FM-theta connectivity and cross-network integration, facilitating learning under low demand while hampering learning under high demand. Significance statement Social anxiety is reliably characterized by biases toward avoidance and aversive learning. Frontal-midline (FM) theta dynamics in the EEG have been proposed as a robust neural marker underlying these biases, yet how FM-theta coordinates large-scale brain networks to support feedback-guided learning remains unclear. Here, we show that elevated levels of social anxiety selectively amplify theta-dependent fronto-occipital connectivity during contextual learning, and that stronger coupling between FM-theta-dependent neural networks predicts better learning performance.

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Publication Details

Journal
Journal of Neuroscience
Published
2026-09-14
DOI
https://doi.org/10.1523/jneurosci.2161-25.2026
Primary Topic
Functional Brain Connectivity Studies
Type
article
Field-Weighted Citation Impact
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article

The cost of scrutiny: subclinical social anxiety and performance context reshape frontal-midline theta network reconfigurations during probabilistic learning

Melle J. W. van der Molen, Hanjie Liu
Journal of Neuroscience
Functional Brain Connectivity Studies
article

The cost of scrutiny: subclinical social anxiety and performance context reshape frontal-midline theta network reconfigurations during probabilistic learning

Melle J. W. van der Molen, Hanjie Liu
article en

Abstract

Social anxiety is reliably characterized by biases toward avoidance and aversive learning. Frontal-midline theta (FM-theta) oscillations have been implicated as a key neural mechanism underlying these learning biases. Here we combined a dynamic network neuroscience approach with computational modeling to investigate how FM-theta oscillatory activity coordinates large-scale functional network interactions on a trial-to-trial basis during feedback-guided learning. Additionally, we examined how these neural dynamics are altered in social anxiety across different social contexts. A sample of 146 human participants (129 female, mean age = 20.4 years) with varying levels of social anxiety completed a probabilistic selection task while performing alone and under scrutiny. Using non-negative matrix factorization, we identified two functional neural subgraphs supported by FM-theta. Fronto-parietal connectivity increased following aversive outcomes and scaled with positive prediction errors, consistent with error-monitoring and belief-updating. Fronto-occipital connectivity scaled with prediction errors when performing alone but not under scrutiny, indicative of context-sensitive disruption of belief-updating. Participants with elevated social anxiety showed increased fronto-occipital connectivity, as well as stronger subgraph coupling, indexing cross-network integration. This latter effect facilitated learning of simple stimulus-reward associations, but hampered learning of difficult stimulus-reward associations. Together, these findings reveal that social anxiety amplifies fronto-occipital FM-theta connectivity and cross-network integration, facilitating learning under low demand while hampering learning under high demand. Significance statement Social anxiety is reliably characterized by biases toward avoidance and aversive learning. Frontal-midline (FM) theta dynamics in the EEG have been proposed as a robust neural marker underlying these biases, yet how FM-theta coordinates large-scale brain networks to support feedback-guided learning remains unclear. Here, we show that elevated levels of social anxiety selectively amplify theta-dependent fronto-occipital connectivity during contextual learning, and that stronger coupling between FM-theta-dependent neural networks predicts better learning performance.

Journal of Neuroscience
Openalex Percentile: Top 9%
Functional Brain Connectivity Studies
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