The superior colliculus arbitrates whole-brain dynamics for unconscious visual insight

Abstract

The human capacity for sudden insight, often marked by abrupt and illuminating "eureka" moments, has long intrigued neuroscientists seeking to understand its elusive neural basis1-6. Mooney image recognition offers a compelling behavioral paradigm of this phenomenon, in which ambiguous black-and-white patterns are abruptly perceived as coherent objects7-13. Whole-brain cortical involvement, which is mainly revealed by the contrast between recognition and nonrecognition, is well established8,14-27. However, the neural dynamics underlying the transition from nonrecognition to recognition, particularly the contributions of noncortical structures, have remained largely unknown. Here, we show that the transition in whole-brain dynamics can be effectively characterized by three large-scale activity patterns and that the superior colliculus (SC) emerges as a structure with a distinct temporal profile that is potentially critical for insight. Using functional clustering of functional magnetic resonance imaging data comprising 41,446 time points from 14 human participants performing this insight task, we identified three distinct functional clusters exhibiting stimulus-driven activation, suppression, and recognition-associated patterns. Notably, the SC in the third cluster displayed a distinct activation peak immediately before the recognition response. Furthermore, empirical dynamic modeling revealed that the SC was the only region in the whole brain that exhibited mutual positive directed interactions with all three clusters and was functionally embedded within higher-order cortical interactions mediating the transformation from stimulus input to motor output. Our findings provide compelling experimental evidence that the SC plays a critical role in orchestrating whole-brain dynamics for sudden insight, calling for a reappraisal of this evolutionarily conserved structure as a key player supporting unconscious but high-level cognitive processing.