Transmedulla Neurons in the Sky Compass Network of the Honeybee (Apis mellifera) Are a Possible Site of Circadian Input.

Maximilian Zeller,Tanja Heinloth,Keram Pfeiffer,Martina Held,Julia Bender,Annuska Berz,Timm Hellfritz,Eric James Warrant

doi:10.1371/journal.pone.0143244

Abstract

Honeybees are known for their ability to use the sun’s azimuth and the sky’s polarization pattern for spatial orientation. Sky compass orientation in bees has been extensively studied at the behavioral level but our knowledge about the underlying neuronal systems and mechanisms is very limited. Electrophysiological studies in other insect species suggest that neurons of the sky compass system integrate information about the polarization pattern of the sky, its chromatic gradient, and the azimuth of the sun. In order to obtain a stable directional signal throughout the day, circadian changes between the sky polarization pattern and the solar azimuth must be compensated. Likewise, the system must be modulated in a context specific way to compensate for changes in intensity, polarization and chromatic properties of light caused by clouds, vegetation and landscape. The goal of this study was to identify neurons of the sky compass pathway in the honeybee brain and to find potential sites of circadian and neuromodulatory input into this pathway. To this end we first traced the sky compass pathway from the polarization-sensitive dorsal rim area of the compound eye via the medulla and the anterior optic tubercle to the lateral complex using dye injections. Neurons forming this pathway strongly resembled neurons of the sky compass pathway in other insect species. Next we combined tracer injections with immunocytochemistry against the circadian neuropeptide pigment dispersing factor and the neuromodulators serotonin, and γ-aminobutyric acid. We identified neurons, connecting the dorsal rim area of the medulla to the anterior optic tubercle, as a possible site of neuromodulation and interaction with the circadian system. These neurons have conspicuous spines in close proximity to pigment dispersing factor-, serotonin-, and GABA-immunoreactive neurons. Our data therefore show for the first time a potential interaction site between the sky compass pathway and the circadian clock.

Highlights

Honeybees possess a time-compensated sun-compass, which enables them to use the solar azimuth, i.e. the horizontal component of the sun’s position, as a reference direction for navigation [1]
Using an antibody against the synaptic vesicle protein synapsin and phalloidin, which binds to filamentous actin, we identified the dorsal rim area of the medulla (MEDRA) as a small neuropil area, at the dorsal edge of the medulla (Fig 1)
Our results show that the sky compass pathway is highly conserved between different insect species

Summary

Introduction

Honeybees possess a time-compensated sun-compass, which enables them to use the solar azimuth, i.e. the horizontal component of the sun’s position, as a reference direction for navigation [1]. Recent evidence from desert ants of the genus Cataglyphis shows that these animals can learn homing directions using only the sun as an orientational cue and later use this information to navigate solely by the polarization pattern and vice versa [9] This suggests that the neuronal correlates of the sun-compass and polarization compass can either exchange information or that they are identical. As polarization-vision systems are normally homochromatic, perception of the color gradient and the direct sun light is performed with the remainder of the compound eye [10, 14] It is currently not clear at which stage of the sky compass pathway these pieces of information are integrated, but electrophysiological data from locusts suggest that a central layer of the medulla might be important for this task [15]

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