A direct auditory subcortical route to the amygdala associated with fear in humans

Rapid and efficient fear processing is essential for survival. In vision, this function is supported by a well-characterized subcortical pathway consisting of direct projections from the pulvinar of the thalamus to the amygdala in the human brain. In contrast, the existence of an analogous shortcut for fear in audition has been demonstrated in non-human animals, but remains unconfirmed in humans. To address this question, we used probabilistic streamline tractography and fixel-based analysis on diffusion-weighted images from Human Connectome Project participants of either sex, to reconstruct candidate auditory subcortical pathways and examine their associations with affective and auditory behavioral measures. Our findings revealed a robust white matter tract connecting the inferior colliculus to basolateral amygdala via the medial geniculate body (MGB) of the thalamus. Remarkably, higher fiber density in this tract was associated with better hearing ability in noise and increased self-reported fearfulness, supporting its role in auditory and affective function. Conversely, a control analysis of the core thalamocortical pathway from ventral MGB to primary auditory cortex (PAC), representing the main route for auditory processing, was associated with auditory ability but not with affective measures. These findings provide previously unreported evidence for an auditory colliculo-geniculo-amygdala "low road" in humans, aligning with evolutionarily conserved pathways for fear described in non-human species.<b>Significance Statement</b> Rapid fear processing is crucial for survival. While a visual subcortical "low road" for fear is well characterized in humans, the existence of an analogous human auditory shortcut remains undetermined. Using diffusion magnetic resonance imaging tractography, we provide evidence for a white matter tract connecting the inferior colliculus to basolateral amygdala via the medial geniculate body of the thalamus, which is associated with hearing ability and self-reported fearfulness. Our findings provide novel evidence for an auditory colliculo-geniculo-amygdala direct route in humans, revealing an evolutionarily conserved pathway for fear previously described in non-human species.