AN AUDITORY “LOW ROAD” FOR THREAT IN HUMANS SENSITIVE TO FAST TEMPORAL CUES: MULTIMODAL INSIGHTS FROM EEG, FMRI, DWI, AND PERIPHERAL MEASURES

Rapid threat processing is crucial for survival. In vision, neural models of emotion propose the existence of direct pathways from visual thalamus to the amygdala, which may rely on magnocellular inputs and enable fast processing of threat signals. In audition, evidence from non-human animals suggests the existence of similar fast magnocellular pathways, but their presence in humans remains unclear. Building on animal evidence that high-amplitude-modulated (highAM) sounds preferentially engage magnocellular auditory processing, we combined physiological and neuroimaging measures to identify a magnocellular pathway for auditory fear in humans. Specifically, we tested whether highAM fear sounds elicit rapid affective responses, and whether highAM emotional processing aligns with auditory thalamo-amygdala anatomical connectivity. During fear conditioning, we recorded electroencephalography and pupillometry (Study I) as well as functional and diffusion-weighted imaging (Study II) from healthy participants as they detected voices. Only stimuli presented at highAM, as opposed to lowAM, elicited early fear-related responses (before 100 ms post-stimulus; study I). Analyses of functional and diffusion-weighted imaging data (Study II) revealed that selective amygdala responses to highAM (and not lowAM) emotional voices were functionally associated with individual fiber density of a direct medial geniculate body – basolateral amygdala pathway. Together, these findings provide convergent functional and anatomical evidence supporting a magnocellular subcortical pathway for auditory threat processing in humans, potentially mirroring the visual subcortical pathways extensively investigated in human emotion research. These results also bridge animal and human work on evolutionarily conserved subcortical systems for affective processing.