Bat eye movements resolve a long-standing question in gaze control

초록

Eye movements enable visual information gathering and stabilize gaze via the optokinetic reflex (OKR) and vestibulo-ocular reflex (VOR) pathways.1 Echolocating bats, despite their rapid and agile flight maneuvers to land upside down and navigate 3D space, have long been thought not to move their eyes, an assumption originating from Walls's influential assertion over 80 years ago2 but never tested with empirical measurements. Here we present a quantitative analysis of eye movements driven by visual and vestibular signals in Seba's short-tailed bat (Carollia perspicillata). Bats generated robust visually driven OKR with an oculomotor range of similar to +/- 10 degrees and displayed strong otolith-mediated responses during off-vertical axis rotation. By contrast, they showed minimal semicircular canal-driven angular VOR (aVOR) for passive head rotations that elicit large, sustained responses in mice. Micro-CT reconstructions revealed that bats and mice have similar semicircular canal geometry, indicating that the weak aVOR does not reflect peripheral anatomical constraints. These findings provide the first empirical demonstration that bats make robust eye movements and exhibit strong visual and otolith-driven components of gaze stabilization. We propose that semicircular canal signals may be more strongly engaged during active flight and modulated by behavioral state-dependent tuning of vestibular pathways to support ecologically specialized behaviors.

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