Mushroom bodies are required for accurate visual navigation in ants

Abstract

Visual navigation in ants has long been a focus of experimental study [1-3], but only recently have explicit hypotheses about the underlying neural circuitry been proposed [4]. Indirect evidence suggests the mushroom bodies (MB), a known site of olfactory learning [5-10], may also be the substrate for visual memory in navigation tasks [11-14]. Computational modelling shows that MB neural architecture could support this function [15, 16], though there is no direct evidence that ants require MBs for visual navigation. Here we show that lesions of MB calyces impair ants' visual navigation to a remembered food location whilst leaving their innate responses to visual cues unaffected. Ants are innately attracted to a large visual cue but we trained them to locate a food source at a specific angle to this visual cue. Subsequent bilateral or unilateral lesioning (through procaine hydrochloride injection) of the MB calyces, caused ants to revert to their innate cue attraction whilst control (saline) injected ants still approached the feeder. The ants' path straightness and walking speed were unaffected by lesions. Reversion towards the cue direction occurred irrespective of whether it was ipsi- or contralateral to the lesion site, showing this is not due simply to an induced motor bias. Monocular occlusion did not diminish ants' ability to locate the feeder, suggesting the lesion is not merely interrupting visual input to the calyx. The demonstrated dissociation between innate and learnt visual responses provides direct evidence for a specific role of the MB in navigational memory.