Distinct subcortical pathways mediate collision detection with and without attention and consciousness

Accurate detection of impending collisions is essential for survival. While multiple subcortical pathways have been found in the detection of looming stimuli, the roles of top-down attention and consciousness in this process remains unclear. Using high-resolution fMRI, we investigated how top-down attention and conscious awareness influence the subcortical processing of collision trajectories in healthy participants and hemianopic patients with cortical blindness. In healthy participants, the superior colliculus (SC)-parabigeminal nucleus (PBGN)-amygdala pathway integrated binocular information for accurate detection of collision trajectories in the upper visual field, but only when participants were paying attention to the looming stimuli. On the other hand, for stimuli presented in the blind visual field of hemianopic patients, effective connectivity analyses revealed collision sensitivity in the SC-pulvinar and SC- ventral tegmental area (VTA) pathways, supporting automatic collision detection even in the absence of visual awareness. Together, these findings suggest that distinct subcortical pathways mediate collision detection in the human brain depending on the presence and absence of attention and conscious awareness. HighlightsO_LIAttention selectively enhanced collision sensitivity in the SCs-PBGN-CMA pathway. C_LIO_LIBinocular information contributed to accurate collision detection in the upper visual field. C_LIO_LISC-Pulvinar and SC-VTA pathways detect collision trajectory without visual awareness. C_LI Significance statementAccurate detection of collision trajectory is critical for survival. Using high-resolution fMRI in healthy participants and hemianopic patients, we show that collision detection is mediated by distinct subcortical circuits depending on the attentional state and conscious awareness. The SC-PBGN-amygdala pathway can precisely detect collision trajectory in upper visual field with top-down attention, whereas the SC-pulvinar and SC-VTA pathways enable automatic collision detection without awareness. These findings reveal distinct functional roles of the subcortical pathways in collision detection.