The influence of stimulus history on directional coding in the monarch butterfly brain

Abstract

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.

Unraveling the neural basis of spatial orientation in arthropods

“…Insights into directional coding by central–complex neurons in monarch butterflies are provided by a study of Jerome Beetz and Basil el Jundi (Beetz and el Jundi 2023 ). The authors have analyzed whether and how spatial tuning of central–complex neurons is affected by different stimulus dynamics, as would occur during turning saccades vs. more slower changes in flight direction.…”

Monarch butterflies memorize the spatial location of a food source

“…While the compass system is a major focus of monarch butterfly research [41][42][43][44][45][58][59][60][61][62][63], there are only a few behavioural studies that investigate the foraging behaviour [48][49][50][51]. Here, we demonstrated that non-migratory monarch butterflies could relocate rewarding feeders by learning spatial information of visual landmarks.…”

Evolution of neural circuitry and cognition

“…Central complex functions overlap strongly with the cognitive processes that generate pollen-feeding behaviour in Heliconius butterflies, where a goal (the location of a pollen resource) is identified, learned and memorized [109]. Subsequently, sensory cues during navigation and foraging, such as optic flow, wind direction, polarized light and recognition of visual features, are integrated and compared with the original goal, and path integration allows the foraging route to be faithfully navigated [102,[110][111][112].…”