Threat imminence modulates neural gain in attention and motor relevant brain circuits in humans

Abstract

Different levels of threat imminence elicit distinct computational strategies reflecting how the organism interacts with its environment in order to guarantee survival. Thereby, parasympathetically driven orienting and inhibition of on-going behavior in post-encounter situations and defense reactions in circa-strike conditions associated with sympathetically driven action preparation are typically observed across species. Here, we show that healthy humans are characterized by markedly variable individual orienting or defense response tendencies as indexed by differential heart rate (HR) changes during the passive viewing of unpleasant pictures. Critically, these HR response tendencies predict neural gain modulations in cortical attention and preparatory motor circuits as measured by neuromagnetic steady-state visual evoked fields (ssVEFs) and induced beta-band (19–30 Hz) desynchronization, respectively. Decelerative HR orienting responses were associated with increased ssVEF power in the parietal cortex and reduced beta-band desynchronization in pre-motor and motor areas. However, accelerative HR defense response tendencies covaried with reduced ssVEF power in the parietal cortex and lower beta-band desynchronization in cortical motor circuits. These results show that neural gain in attention- and motor-relevant brain areas is modulated by HR indexed threat imminence during the passive viewing of unpleasant pictures. The observed mutual ssVEF and beta-band power modulations in attention and motor brain circuits support the idea of two prevalent response tendencies characterized by orienting and motor inhibition or reduced stimulus processing and action initiation tendencies at different perceived threat imminence levels.