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Readers move their eyes mindlessly using midbrain visuo-motor principles

Vitu, F.; Adeli, H.; Zelinsky, G. J.

2021-10-22 neuroscience
10.1101/2021.10.21.465242 bioRxiv
Show abstract

Saccadic eye movements rapidly shift our gaze over 100,000 times daily, enabling countless tasks ranging from driving to reading. Long regarded as a window to the mind1 and human information processing2, they are thought to be cortically/cognitively controlled movements aimed at objects/words of interest3-10. Saccades however involve a complex cerebral network11-13 wherein the contribution of phylogenetically older sensory-motor pathways14-15 remains unclear. Here we show using a neuro-computational approach16 that mindless visuo-motor computations, akin to reflexive orienting responses17 in neonates18-19 and vertebrates with little neocortex15,20, guide humans eye movements in a quintessentially cognitive task, reading. These computations occur in the superior colliculus, an ancestral midbrain structure15, that integrates retinal and (sub)cortical afferent signals13 over retinotopically organized, and size-invariant, neuronal populations21. Simply considering retinal and primary-visual-cortex afferents, which convey the distribution of luminance contrast over sentences (visual-saliency map22), we find that collicular population-averaging principles capture readers prototypical word-based oculomotor behavior2, leaving essentially rereading behavior unexplained. These principles reveal that inter-word spacing is unnecessary23-24, explaining metadata across languages and writing systems using only print size as a predictor25-26. Our findings demonstrate that saccades, rather than being a window into cognitive/linguistic processes, primarily reflect rudimentary visuo-motor mechanisms in the midbrain that survived brain-evolution pressure27.

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