An auditory "low road" for threat in humans sensitive to fast temporal cues

Abstract

Rapid threat processing is crucial for survival. In vision, neural models of emotion propose the existence of direct pathways, or "low roads", from visual thalamus to the amygdala, which may rely on magnocellular inputs and thereby enable rapid processing of threat signals. In audition, evidence from non-human animals points to the existence of a similar fast direct pathway, but its presence in humans remains unknown. Building on animal evidence that high-rate amplitude-modulated (highAM) sounds preferentially engage magnocellular processing, we used behavioral, physiological, and neuroimaging measures to search for an auditory "low road" for threat in humans responsive to magnocellular-associated features. Specifically, we tested whether highAM threat cues elicit rapid affective responses, and whether highAM threat processing aligns with structural thalamo-amygdala connectivity. We recorded electroencephalography and pupillometry from participants while they detected voices during fear conditioning. Emotional voices presented at highAM rates, as opposed to lowAM, elicited threat-related responses during the earliest post-stimulus window. A further study combining functional and diffusion-weighted imaging revealed that selective amygdala responses to highAM threatening voices were functionally associated with individual fiber density of an auditory thalamo-amygdala pathway. These results provide convergent functional and anatomical evidence supporting a subcortical pathway for auditory threat processing, consistent with evolutionarily conserved emotional systems.