Processing of sky compass signals at different stages of the polarization-vision pathway in the brain of the desert locust (Schistocerca gregaria)

Although insect brains are small in comparison to those of vertebrates, some species show astonishing navigational abilities. Desert locusts (Schistocerca gregaria) are well-known for forming huge swarms consisting of millions of animals and their long-range migrations throughout North Africa and the Middle East. Experiments on tethered flying locusts showed that the animals respond with a 180°-periodicity of yaw-torque to a dorsally rotating polarizer. This suggests that locusts are able to use celestial polarized light as navigational cue during spatial orientation and navigation. A number of recent studies have explored the neural basis of sky compass orientation in locusts by focusing on the processing of polarized light signals in the brain. In contrast, (1) the mechanisms of compensation for changes of solar position over the course of the day and (2) the integration of different signals from the sky (polarization pattern, solar position, chromatic gradient) are poorly understood, particularly at the level of the optic lobe. Finally, (3) no data exist comparing the sky compass system in diurnal gregarious locusts with that of nocturnal solitarious locusts. Towards these goals, polarization-sensitive neurons at different levels of the polarization vision pathway were analyzed physiologically through intracellular recordings and anatomically by means of detailed three-dimensional reconstructions of neuronal arborizations. First, neurons of the medulla in the optic lobe were analyzed and characterized to understand the combination and integration of sky compass information in the locust brain. These experiments showed that neurons of a distinct layer of the medulla (layer 4) integrate polarized light information from the dorsal rim area of the compound eye in the locust brain. In addition, all polarization-sensitive neurons responded also to an unpolarized green/UV light spots that moved around the locust head. Taken together, this chapter shows that neurons of medulla layer 4 combine polarized light information of the sky with azimuth-dependent unpolarized light input that might represent celestial chromatic contrast information. In the next chapter, receptive field properties and responses of neurons to different light intensity conditions were studied. These investigations focused on neurons of the anterior optic tubercle – the next processing stage of the polarization pathway – and compared the physiology of these neurons in gregarious and solitarious locusts. The data showed that both locust phases rely on the same sky navigation system, although they have strikingly different life styles. The experiments revealed novel aspects of the response characteristics of intertubercle neurons and a possible modulatory role of the LoTu1 neuron in the anterior optic tubercle in both locust phases. In the third chapter, evidence for a second polarization vision pathway in the brain is presented. This pathway connects the dorsal rim area of the medullae via the accessory medullae to the central complex and might provide time-compensated polarized light signals to the central complex. Finally, chapter four presents a standardized three-dimensional atlas of the central complex and reveals a possible connection between a particular type of polarization-sensitive columnar neuron and a neuron that is modulated during flight. This chapter illustrates how the polarization-vision network of the central complex might be modulated in a context-dependent manner.