Sound activates a dormant visual-motor pathway bypassing primary visual cortex

Like in other species, the primate visual system contains an anatomical retinal projection bypassing the geniculostriate pathway and innervating the midbrain. However, unlike in some of these species, the functional significance of this alternative visual pathway remains unknown: increasing evidence suggests that it may be completely dormant. We first tested this by performing focal, reversible inactivation of the primary visual cortex (V1) and investigating a short-latency oculomotor reflex believed to rely on subcortical eye-movement control circuits. This reflex, called saccadic inhibition (recently reviewed by Buonocore and Hafed, 2023), is characterized by a short-latency inhibition of saccade generation by visual stimuli, as well as by a concomitant saccade direction biasing, first towards and then away from stimulus location. When we created a localized cortical scotoma, saccadic inhibition was completely abolished for stimuli in the blind field, confirming the geniculostriate pathway’s dominance. Superior colliculus visual responses were also eliminated. However, why does the alternative visual pathway, directly targeting oculomotor control circuits, exist at all? We hypothesized that this pathway might still be functional, albeit in a gated manner. During V1 inactivation, we paired a visual onset with a sound pulse (50 ms; 1 KHz; suprathreshold) that was completely uninformative about the visual stimulus’ location. Saccadic inhibition was partially restored, and it was different to when the sound pulse occurred alone. Most importantly, there was a re-emergence of saccade direction biasing towards the visual stimulus location, even though the sound was not spatially informative. Guessed visually-guided saccades towards a target presented in the blind field were also mildly more accurate with the uninformative sound. These results demonstrate that multi-sensory information can activate an otherwise dormant visual-motor pathway. These results also highlight the importance of multi-species comparisons of hierarchical sensory-motor processes, and they especially inform models of active sensory-guided behavior invoking parallel processing streams.