Experience-related reorganization of giant synapses in the lateral complex: Potential role in plasticity of the sky-compass pathway in the desert ant Cataglyphis fortis.

Cataglyphis desert ants undergo an age-related polyethism from interior workers to relatively short-lived foragers with remarkable visual navigation capabilities, predominantly achieved by path integration using a polarized skylight-based sun compass and a stride-integrating odometer. Behavioral and physiological experiments revealed that the polarization (POL) pattern is processed via specialized UV-photoreceptors in the dorsal rim area of the compound eye and POL sensitive optic lobe neurons. Further information about the neuronal substrate for processing of POL information in the ant brain has remained elusive. This work focuses on the lateral complex (LX), known as an important relay station in the insect sky-compass pathway. Neuroanatomical results in Cataglyphis fortis show that LX giant synapses (GS) connect large presynaptic terminals from anterior optic tubercle neurons with postsynaptic GABAergic profiles of tangential neurons innervating the ellipsoid body of the central complex. At the ultrastructural level, the cup-shaped presynaptic structures comprise many active zones contacting numerous small postsynaptic profiles. Three-dimensional quantification demonstrated a significantly higher number of GS (∼ 13%) in foragers compared with interior workers. Light exposure, as opposed to age, was necessary and sufficient to trigger a similar increase in GS numbers. Furthermore, the increase in GS numbers was sensitive to the exclusion of UV light. As previous experiments have demonstrated the importance of the UV spectrum for sky-compass navigation in Cataglyphis, we conclude that plasticity in LX GS may reflect processes involved in the initial calibration of sky-compass neuronal circuits during orientation walks preceding active foraging.