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Tree shrews combine panoramic vision with an expanded oculomotor repertoire

Ratnadeep Pal, Erin KempkesiD, Rishi Aeleti, Elizabeth Tubbs, Arnab BiswasiD, Madineh Sedigh-SarvestaniiD

Abstract

Mammals differ in how they redirect gaze. Primates shift and hold gaze with rapid, precise eye movements that can be decoupled from the head. In lateral-eyed mammals studied to date, gaze is organized around the head: saccades are coupled to head rotation in freely moving animals and typically accompanied by attempted head movements even under head fixation. These observations suggest a trade-off: animals that keep a panoramic field give up the precise, eye-driven control of gaze typical of frontal-eyed animals. But because lateral eyes and head-centered gaze co-occur in every lateral-eyed species studied, it is unknown whether one follows from the other. Here we test this in the tree shrew, an arboreal mammal with laterally placed eyes. Using real-time eye tracking in head-fixed animals, we find that tree shrews saccade frequently under head fixation and that most saccades occur without detectable attempted head movement. Tree shrews make visually evoked saccades, along both the horizontal and vertical axes of the visual field, toward targets. They can also fixate on visual targets. Using widefield calcium imaging, we show that visual cortex over-represents the central visual field. Lastly, we show that extraocular muscles that move the eyes contain specialized nerve endings found in frontal-eyed species. Based on this suite of evidence, we conclude that lateral eyes do not preclude eye-driven gaze control. The two are separable dimensions of visual system design, a combination that may suit animals whose locomotion routinely points the head away from where they need to look.

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02 /Specification & Classification

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