Neural Integration Underlying a Time-Compensated Sun Compass in the Migratory Monarch Butterfly

Abstract

Migrating Eastern North American monarch butterflies use a time-compensated sun compass to adjust their flight to the southwest direction. While the antennal genetic circadian clock and the azimuth of the sun are instrumental for proper function of the compass, it is unclear how these signals are represented on a neuronal level and how they are integrated to produce flight control. To address these questions, we constructed a receptive field model of the compound eye that encodes the solar azimuth. We then derived a neural circuit model, which integrates azimuthal and circadian signals to correct flight direction. The model demonstrates an integration mechanism, which produces robust trajectories reaching the southwest regardless of the time of day and includes a configuration for remigration. Comparison of model simulations with flight trajectories of butterflies in a flight simulator shows analogous behaviors and affirms the prediction that midday is the optimal time for migratory flight.

The insect central complex and the neural basis of navigational strategies

“…Alternatively, the output of the entire circuit could be modulated according to time of day. While a recent study models how the Sun-compass may be time compensated (Shlizerman et al, 2016), it does not suggest a specific neural substrate and it remains to be shown whether the neural circuitry for representing current and desired headings is involved in azimuth compensation.…”

Demystifying Monarch Butterfly Migration

“…noted, is a biologically tangible clock-to-compass circuit. Thus, a working mathematical model of the time-compensated sun compass has been proposed [51]. For this model, a receptive field of the compound eye that encodes solar azimuth was first constructed.…”

Bio-inspired navigation algorithm for GPS denial modes

“…The comparison of the sun sensors from Solar MEMS technologies are given in the following The field of view of these sensors is limited to ±60º which will not be able to cover the full spectrum for our application. To resolve this issue, five sensors can be used with the mounting shown in Figure 3 A majority of animal species including migrating Eastern North American monarch butterflies has the vision mediated by compound eyes [11] [16]. Floreano [16] have succeeded in fabricating a prototype of a miniature curved artificial compound eye named CurvACE which can calculate the solar azimuth based on photodetectors.…”

“…The physical model they implemented uses the visual inputs from the structure based on Dorsal Rim Area (DRA) along with the temporal circadian rhythm and the polarization pathway where the combination of detected relative bearing from the sun and predicted sun azimuth is used to calculate absolute heading. [5] In the studies of migrating Eastern North American monarch butterflies performed by Shlizerman [11], they present a model that integrates neuronal oscillations of the sun's horizontal position and the circadian clock to direct flight and their model explains flight simulator tracks and proposes a space-time integration mechanism for directional flight. The monarchs use a circadian clock housed in the antennae which is capable of keeping track of time-of-day and to control the sun compass timings.…”

“…The results of their study demonstrates a simple neuronal integration mechanism based on matching spiking rates of clock and azimuth neural signals to provide angular position control and this mechanism helps monarch butterflies to make their journey and reach their overwintering sites relying on limited food sources on their flight path. [11] The basic idea of this project is to calibrate the observer's position when the azimuth and zenith/incidence angles for the sun's position are known. The solar position algorithms available calculate the azimuth and zenith/incidence angles for the sun's position at any given point of time when the position of the observer is known.…”