Abstract
Navigating into the unknown: Multimodal Orientation in Monarch Butterflies
Long distance migration in animals requires robust neural mechanisms for encoding and integrating multiple environmental cues. Monarch butterflies (Danaus plexippus), which travel thousands of kilometers from North America to Central Mexico each fall, provide a powerful model for uncovering the neuronal foundations of natural orientation behaviors. We show that migrating Monarchs rely on a hierarchy of compass cues: under natural skies, they maintain stable southward headings, primarily guided by the solar azimuth. When the sun is obscured, Monarchs instead orient using the celestial polarization pattern. Strikingly, even in the absence of both sun and polarized light, these insects preserve their migratory direction, revealing a fallback mechanism based on sensing the celestial intensity gradient and/or the Earth’s magnetic field. While previous study indeed provide evidence that Monarch butterflies are sensitive to changes in magnetic fields, the neuronal basis by which insects detect and encode the Earth’s magnetic field remains completely unknown. Moreover, it is unclear how the Earth’s magnetic field is combined with other celestial cues, such as the sun and polarized light.
To address this gap, we developed a magnetically inert tetrode recording setup in which tethered Monarch butterflies can actively navigate at the center of a double wrapped 3D-Helmholtz-coil. This enables controlled magnetic stimulation during extracellular recordings. We focus on the central complex, the brain region in the insect brain known to encode spatial orientation to identify neurons involved in magnetic and multimodal compass processing during active orientation. By combining behavioral cue manipulation experiments with magnetic free neurophysiology, this integrated approach provides a comprehensive framework for uncovering how the Monarch’s brain encodes a multimodal compass. These advances will pave the way for resolving the neural mechanisms underlying magnetic sensing and for understanding how natural behaviors emerge from dynamic, multimodal sensory integration.