A retinal code for motion along the gravitational and body axes

• Published in: Nature (London) 2017-06, Vol.546 (7659), p.492-497
• Main Authors: Sabbah, Shai, Gemmer, John A., Bhatia-Lin, Ananya, Manoff, Gabrielle, Castro, Gabriel, Siegel, Jesse K., Jeffery, Nathan, Berson, David M.
• Format: Article
• Language: English
• Subjects: 13/1; 13/44; 14/19; 14/34; 14/35; 14/69; 631/378/2613/1483; 631/378/2613/1786; 631/378/2617/1780; 631/378/2629/1779; 631/378/3917; 64/60; 9/74; Animals; Female; Gravitation; Humanities and Social Sciences; Male; Mice; Motion perception (Vision); Movement (Physiology); multidisciplinary; Neurons; Observations; Ocular Physiological Phenomena; Optic Flow - physiology; Physiological aspects; Physiological research; Postural Balance - physiology; Retina; Retinal Ganglion Cells - physiology; Rotation; Science; Space Perception - physiology; Vestibule, Labyrinth - physiology; Visual pathways
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature22818

Self-motion triggers complementary visual and vestibular reflexes supporting image-stabilization and balance. Translation through space produces one global pattern of retinal image motion (optic flow), rotation another. We examined the direction preferences of direction-sensitive ganglion cells (DSGCs) in flattened mouse retinas in vitro . Here we show that for each subtype of DSGC, direction preference varies topographically so as to align with specific translatory optic flow fields, creating a neural ensemble tuned for a specific direction of motion through space. Four cardinal translatory directions are represented, aligned with two axes of high adaptive relevance: the body and gravitational axes. One subtype maximizes its output when the mouse advances, others when it retreats, rises or falls. Two classes of DSGCs, namely, ON-DSGCs and ON-OFF-DSGCs, share the same spatial geometry but weight the four channels differently. Each subtype ensemble is also tuned for rotation. The relative activation of DSGC channels uniquely encodes every translation and rotation. Although retinal and vestibular systems both encode translatory and rotatory self-motion, their coordinate systems differ. Global mapping shows that mouse retinal neurons prefer visual motion produced when the animal moves along two behaviourally relevant axes, allowing the encoding of the animal’s every translation and rotation. All eyes on motion encoding The local wiring that allows some retinal neurons to detect motion direction in visual stimuli has been well studied, but how their ensemble encodes optic flow more generally has not. Now David Berson and colleagues have performed a global mapping of direction preferences in mouse direction-sensitive ganglion cells (DSGCs) and show that they align with just two ethologically relevant axes: the body axis and the gravitational axis. Relative activation of the sixteen resulting channels, that is four cardinal directions multiplied by two DSGC types (ON vs ON-OFF) for two eyes, allows for the unique encoding of every translation and rotation associated with the animal's self-motion. This creates a visual feedback that complements the bio-mechanical vestibular system in controlling image stabilization and balance.