BOLD signals of learning dynamics across and within trials beyond the classical fear and extinction network

Abstract

Human functional magnetic resonance imaging studies of fear conditioning often average neural responses across trials, potentially obscuring transient activations that vary across learning. In this study with 139 participants, we examined finer temporal dynamics of conditioned responding by analyzing three 2s segments within the conditioned stimulus (CS) presentation period across each quarter of fear acquisition and extinction training. This approach revealed distinct, time-specific engagement of regions within fear- and safety-related networks, both within and across trials. In particular, different activation patterns emerged across the three trial segments during CS presentation, indicating that neural responses were not limited to CS onset. We observed a more classical activation pattern at 0s relative to CS onset that diverged in later trial segments, most notably involving the amygdala, hippocampus, and prefrontal cortex (PFC) structures such as vmPFC present exclusively in 2s and 4s trial segments. We also found sustained activations consistent across all blocks of trials, such as right vlPFC activation 4s after CS onset across all fear acquisition quarters. These findings suggest that conditioned fear and safety processing unfold as dynamic spatiotemporal cascades and highlight the importance of modeling later responses following CS onset rather than focusing exclusively on onset-related activation.