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Encoding a time-compensated sun compass

Subject Area Cognitive, Systems and Behavioural Neurobiology
Term from 2016 to 2023
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 317616350
 
Final Report Year 2023

Final Report Abstract

Every autumn, millions of Monarch butterflies (Danaus plexippus) migrate thousands of kilometers from North America to their overwintering habitats in Central Mexico. To migrate in the correct southerly direction, they use external references that allow them to set and keep a constant direction. One obvious source of directional information that can be used in unfamiliar areas is the sun. In addition, additional celestial cues, such as polarized light, are used by many insects, and can potentially help Monarch butterflies keep their direction during migration. Using celestial cues as orientation references to navigate in a consistent compass direction poses one major problem: while the migratory destination is a stationary location, skylight cues change their positions throughout the course of a day. To successfully reach their destination, they must therefore somehow adjust their heading relative to the sun’s position in a time of day-dependent manner. This Emmy Noether project set out to unravel the sun compass of Monarch butterflies and how it is compensated by the modality “time”. Using behavioral flight simulator experiments, we found that these animals use the polarized skylight information as an orientation reference. In addition, we found that the butterflies respond to a change in the Earth’s magnetic field, suggesting that the butterflies rely on multimodal sensory inputs during migration. Through indoor flight simulators, we also found evidence that the sun and polarized light are sufficient cues to trigger the migratory flight directions in migrating butterflies. We further designed a novel flight simulator that allowed us to show the relevance of panoramic and celestial cues and to reveal different orientation strategies in Monarch butterflies. Through intracellular recordings, we characterized the eyes of the butterflies and found green, blue, and UV sensitive photoreceptors as well as indirect evidence for red sensitive photoreceptors. We characterized the neurons of the central-complex, the internal compass in the butterfly’s brain, in migratory and non-migratory butterflies with the main focus of input neurons. We found that these cells integrate different visual cues (sun, polarized light, panoramic scenes) and are tuned differently in migratory butterflies, allowing these butterflies to keep their southerly migratory direction with the highest efficiency. In addition, we discovered a new class of compass neuron that seems to be lepidopteran-specific and might be suitable to be involved in the time-compensation of the sun compass. In addition, we have established a tetrode recording setup that enabled us to record from the compass in tethered flying butterflies, while simultaneously observing the animal’s orientation behavior. This allowed us to study the butterfly’s compass for the first time under different behavioral stages (e.g. quiescent vs. walking, vs. flight) and revealed how the coding of the sun alters during locomotion. We characterized the central-complex network in detail and found that this brain region houses headdirection, goal-direction, and steering neurons. We have successfully performed long-term recordings from central-complex neurons in nature and found, for the first time, evidence for time compensation in the butterfly’s central complex. Taken together, we have investigated the use of the celestial and terrestrial cues in Monarch butterflies in detail and revealed novel insights into the brain network of migration.

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