Anxious vision: Trait-like visual cortical hyperactivity in trait anxiety

Abstract

Sensory processing varies across individuals, often manifesting as distinct traits. Some traits, particularly sensory hypersensitivity, even to basic non-valenced stimuli, are closely linked to emotional traits and implicated in a diversity of psychiatric disorders. Extant theories attribute this sensory-emotion linkage to limbic and prefrontal modulation, but empirical support remains limited. Meanwhile, it is increasingly recognized that sensory cortex supports flexible, value-based processing beyond labeled-line sensory analysis. Assaying early visual cortical activity (using visual evoked potentials/VEPs) across four high-density electroencephalogram (hd-EEG) experiments, involving three independent samples (N = 150) and repeated assessments (up to three waves), we identify a reliable and generalizable pattern of visual cortical hyperactivity related to high trait anxiety. Notably, this effect was specific to the parvocellular (vs. magnocellular) pathway, emerging as early as 46 ms and localized to V1. Underscoring its trait-like stability, the effect was reproducible across different arousal states, neutral and negative stimuli, extended time intervals, and varied experimental paradigms. Moreover, its ecological validity was affirmed by its presence in response to both basic low-level stimuli (Gabor patches) and complex real-world images. Crucially, an excitation-inhibition (E/I) ratio (indexed by the resting-state EEG aperiodic exponent; 1/f slope) predicted parvocellular VEP magnitude in subjects with low but not high trait anxiety, suggesting disrupted E/I modulation in trait anxiety underpins this hyperactivity. We conclude that in trait anxiety, early visual processing deviates from strict "fidelity" to physical-world input or mere "subservience" to top-down modulation, instead adapting to an individuals biological propensity at the earliest processing stage. HighlightsO_LIHyperactivity in primary visual cortex is stable, trait-like C_LIO_LIIt occurs as early as 46 ms post-stimulus, during initial feedforward sweep C_LIO_LIIt covaries with trait anxiety, a key personality factor and risk predisposition for psychiatric disorders C_LIO_LIIt is related to disrupted excitation-inhibition modulation of visual cortex in trait anxiety C_LI