Visual navigation in ants has long been a focus of experimental study [1][2][3], but only recently have explicit hypotheses about the underlying neural circuitry been proposed [4]. Indirect evidence suggests the mushroom bodies (MB) may be the substrate for visual memory in navigation tasks [5-8],

12 13 KEY WORDS 14 Visual navigation, innate visual behaviour, neural circuitry, mushroom body, brain lesions, procaine 15 hydrochloride, wood ants, Formica rufa, insects 16 17 SUMMARY 18Visual navigation in ants has long been a focus of experimental study [1][2][3], but only recently 19 have explicit hypotheses about the underlying neural circuitry been proposed [4]. Indirect evidence 20 suggests the mushroom bodies (MB), a known site of olfactory learning [5][6][7][8][9][10], may also be the 21 substrate for visual memory in navigation tasks [11][12][13][14]. Computational modelling shows that MB 22 neural architecture could support this function [15, 16], though there is no direct evidence that ants 23 require MBs for visual navigation. Here we show that lesions of MB calyces impair ants' visual 24 navigation to a remembered food location whilst leaving their innate responses to visual cues 25 unaffected. Ants are innately attracted to a large visual cue but we trained them to locate a food source 26 at a specific angle to this visual cue. Subsequent bilateral or unilateral lesioning (through procaine 27 hydrochloride injection) of the MB calyces, caused ants to revert to their innate cue attraction whilst 28 control (saline) injected ants still approached the feeder. The ants' path straightness and walking 29 speed were unaffected by lesions. Reversion towards the cue direction occurred irrespective of 30 whether it was ipsi-or contralateral to the lesion site, showing this is not due simply to an induced 31 motor bias. Monocular occlusion did not diminish ants' ability to locate the feeder, suggesting the 32 lesion is not merely interrupting visual input to the calyx. The demonstrated dissociation between 33 innate and learnt visual responses provides direct evidence for a specific role of the MB in 34 navigational memory. 35 36 RESULTS AND DISCUSSION 37Ants learn to navigate to a food source relative to a visual cue 38 Wood ant (Formica rufa) foragers were placed at the centre of a circular platform within a 39 large, circular white arena ( Figure 1A). A large black rectangular cue was mounted on the wall of the 40 arena. Foragers were innately attracted to the cue, walking towards it ( Figure S1A). We then trained 41 foragers to find food located at the edge of a circular platform placed 30° to the right of the cue 42 ( Figure 1B). After 3.8 ± 1.1 days (mean ± SD) days of training, the ants' direction relative to the cue 43 had shifted significantly (Watson Williams test, p<0.001) and they walked directly towards the feeder 44 ( Figure S1B). This demonstrates that ants can visually navigate to a food source, overriding their 45 innate attraction to the visual cue. 46 47 Mushroom bodies (MBs) are required for accurate visual navigation 48We investigated the role of the ants' mushroom bodies during this visual navigation task by 49 making chemical lesions through the injection of procaine hydrochloride, a local anaesthetic that 50 silences neural activity by reversibly blocking voltage-gated channels, includ...

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