Specialized parallel pathways for adaptive control of visual object pursuit

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Abstract

To pursue an unpredictably moving visual object, the brain must generate motor commands that continuously steer the object to the midline of the visual field via feedback. Behavior implies that visual pursuit relies on a feedback loop with flexible gain, but the mechanisms of this “adaptive control” are not well-understood. Here we show that adaptive control in the Drosophila pursuit system involves two parallel feedback loops. One serves to steer the object coarsely toward the midline; the properties of this pathway are relatively constant. The other functions to steer the object precisely to the midline, and its properties are flexible: gain increases when the object is moving away from the midline, when the pursuer is running fast, and during arousal. Genetically suppressing this flexible pathway decreases pursuit performance in aroused males. Our findings show how biological feedback systems can implement adaptive control to drive vigorous error correction while avoiding instability.

Highlights

  • Parallel pathways detect a visual object in the frontal versus lateral visual field

  • Steering arises from combined ipsilateral excitation and contralateral inhibition

  • The circuit for frontal objects is direction-selective, for anticipatory steering

  • The circuit for frontal objects is also recruited during fast running and arousal

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