Migratory animals can detect and use the Earth's magnetic field for orientation and navigation, sometimes over distances spanning thousands of kilometers. How they do so remains, however, one of the greatest mysteries in all sensory biology. Here, the author reviews the progress made to understand the molecular bases of the animal magnetic sense focusing on insect species, the only species in which genetic studies have so far been possible. The central hypothesis in the field posits that magnetically sensitive radical pairs formed by photoexcitation of cryptochrome proteins are key to animal magnetoreception. The author provides an overview of our current state of knowledge for the involvement of insect light-sensitive type I and light-insensitive type II cryptochromes in this enigmatic sense, and highlights some of the unanswered questions to gain a comprehensive understanding of magnetoreception at the organismal level.
The representation and integration of internal and external cues is crucial for any organism to execute appropriate behaviors. In insects, a highly conserved region of the brain, the central complex (CX), functions in the representation of spatial information and behavioral states, as well as the transformation of this information into desired navigational commands. How does this relatively invariant structure enable the incorporation of information from the diversity of anatomical, behavioral, and ecological niches occupied by insects? Here, we examine the input channels to the CX in the context of their development and evolution. Insect brains develop from ~ 100 neuroblasts per hemisphere that divide systematically to form "lineages" of sister neurons, that project to their target neuropils along anatomically characteristic tracts. Overlaying this developmental tract information onto the recently generated Drosophila "hemibrain" connectome and integrating this information with the anatomical and physiological recording of neurons in other species, we observe neuropil and lineage-specific innervation, connectivity, and activity profiles in CX input channels. We posit that the proliferative potential of neuroblasts and the lineage-based architecture of information channels enable the modification of neural networks across existing, novel, and deprecated modalities in a species-specific manner, thus forming the substrate for the evolution and diversification of insect navigational circuits.
The central complex is a brain region in the insect brain that houses a neural network specialized to encode directional information. Directional coding has traditionally been investigated with compass cues that revolve in full rotations and at constant angular velocities around the insect's head. However, these stimulus conditions do not fully simulate an insect's sensory perception of compass cues during navigation. In nature, an insect flight is characterized by abrupt changes in moving direction as well as constant changes in velocity. The influence of such varying cue dynamics on compass coding remains unclear. We performed long-term tetrode recordings from the brain of monarch butterflies to study how central complex neurons respond to different stimulus velocities and directions. As these butterflies derive directional information from the sun during migration, we measured the neural response to a virtual sun. The virtual sun was either presented as a spot that appeared at random angular positions or was rotated around the butterfly at different angular velocities and directions. By specifically manipulating the stimulus velocity and trajectory, we dissociated the influence of angular velocity and direction on compass coding. While the angular velocity substantially affected the tuning directedness, the stimulus trajectory influenced the shape of the angular tuning curve. Taken together, our results suggest that the central complex flexibly adjusts its directional coding to the current stimulus dynamics ensuring a precise compass even under highly demanding conditions such as during rapid flight maneuvers.
The optic flow, i.e., the displacement of retinal images of objects in the environment induced by self-motion, is an important source of spatial information, especially for fast-flying insects. Spatial information over a wide range of distances, from the animal's immediate surroundings over several hundred metres to kilometres, is necessary for mediating behaviours, such as landing manoeuvres, collision avoidance in spatially complex environments, learning environmental object constellations and path integration in spatial navigation. To facilitate the processing of spatial information, the complexity of the optic flow is often reduced by active vision strategies. These result in translations and rotations being largely separated by a saccadic flight and gaze mode. Only the translational components of the optic flow contain spatial information. In the first step of optic flow processing, an array of local motion detectors provides a retinotopic spatial proximity map of the environment. This local motion information is then processed in parallel neural pathways in a task-specific manner and used to control the different components of spatial behaviour. A particular challenge here is that the distance information extracted from the optic flow does not represent the distances unambiguously, but these are scaled by the animal's speed of locomotion. Possible ways of coping with this ambiguity are discussed.
