Vertical Lobes of the Mushroom Bodies are Essential for View-Based Navigation in Australian Bull Ants

Abstract

For many animals, visual landmarks provide information about their location in space and the direction to a goal. Insects acquire this visual information through a series of well-choreographed walks or flights of learning carried out prior to leaving home. Views acquired during learning walks are sufficient for pinpointing goals both when in their vicinity and when animals are at locations they have not visited previously. It is presumed that animals returning home match the memorised views to their current view for successful view-based navigation. While view-based navigation strategies have been incorporated in a wide variety of navigation models used in robotics, we still know very little about how view-based navigation is performed by the insect brain. We investigated the role of the mushroom bodies in view-based navigation in a visually oriented Australian bull ant Myrmecia midas. We targeted the mushroom body vertical lobes (VL) because they are innervated by the visual input regions of the mushroom body and are known to be involved in learning and memory. To ensure that ants in our experiments could navigate using only visual landmarks, we captured experienced foragers close to their nest when they were returning home. For our treatment group, we selectively inhibited neural activity in the VL of the mushroom bodies using the anesthetic procaine and compared their behaviour with three groups: untreated control, VL saline injected, and off-target (antennal lobe) procaine injected groups. Ants were then released at their familiar foraging tree, their subsequent paths were filmed, and their final destinations were determined. While all groups exhibited similar walking speeds, we found significant differences in their orientation and the ability of ants to successfully return home. Untreated control and off-target procaine injected ants were well directed and the most successful at returning home. Animals with procaine-inactivated VL had tortuous paths with multiple loops and were unable to find their nest. We analysed their walking speed relative to gaze direction and found that untreated animals accelerated when their gaze was directed toward home. This behaviour was eliminated by anaesthetizing the VL. Our data show that a simple and effective view-based navigation strategy – accelerate whenever a homeward view is in the frontal visual field – is mediated by the VL of the ant brain. We therefore provide neurobiological evidence that view-based navigation requires functional mushroom bodies.