A Distinct Layer of the Medulla Integrates Sky Compass Signals in the Brain of an Insect

Basil El Jundi,Keram Pfeiffer,Uwe Homberg,Wulfila Gronenberg

doi:10.1371/journal.pone.0027855

Basil El Jundi, Keram Pfeiffer + Show 2 more

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https://doi.org/10.1371/journal.pone.0027855

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Journal: PLoS ONE	Publication Date: Nov 16, 2011
Citations: 92	License type: CC BY 4.0

Affiliation: Dalhousie University, Philipps University of Marburg

Abstract

Mass migration of desert locusts is a common phenomenon in North Africa and the Middle East but how these insects navigate is still poorly understood. Laboratory studies suggest that locusts are able to exploit the sky polarization pattern as a navigational cue. Like other insects locusts detect polarized light through a specialized dorsal rim area (DRA) of the eye. Polarization signals are transmitted through the optic lobe to the anterior optic tubercle (AOTu) and, finally, to the central complex in the brain. Whereas neurons of the AOTu integrate sky polarization and chromatic cues in a daytime dependent manner, the central complex holds a topographic representation of azimuthal directions suggesting a role as an internal sky compass. To understand further the integration of sky compass cues we studied polarization-sensitive (POL) neurons in the medulla that may be intercalated between DRA photoreceptors and AOTu neurons. Five types of POL-neuron were characterized and four of these in multiple recordings. All neurons had wide arborizations in medulla layer 4 and most, additionally, in the dorsal rim area of the medulla and in the accessory medulla, the presumed circadian clock. The neurons showed type-specific orientational tuning to zenithal polarized light and azimuth tuning to unpolarized green and UV light spots. In contrast to neurons of the AOTu, we found no evidence for color opponency and daytime dependent adjustment of sky compass signals. Therefore, medulla layer 4 is a distinct stage in the integration of sky compass signals that precedes the time-compensated integration of celestial cues in the AOTu.

Highlights

Many insects show impressive navigational skills during homing and seasonal migrations [1,2]
Polarization-sensitive neurons in the optic lobe To analyze the processing of polarized light signals in the optic lobe, neurons of the medulla were studied through intracellular recordings combined with dye injections
Ramifications of all neurons in medulla layer 4 suggest that this layer integrates signals from the polarization pattern of the sky with unpolarized celestial cues for sky compass signaling

Summary

Introduction

Many insects show impressive navigational skills during homing and seasonal migrations [1,2]. The sun is often the most important directional cue It is the brightest spot in the sky and gives rise to a characteristic pattern of polarization (Fig. 1A) and chromatic contrast across the sky. Desert locusts detect polarized light with photoreceptors located in a specialized dorsal rim area (DRA) of the compound eye [5,6]. DRA photoreceptors are adapted for high polarization sensitivity and transmit polarization information to dorsal rim areas of the lamina and medulla in the optic lobe. Polarization-sensitive (POL) interneurons respond with sinusoidal modulation of firing rate during zenithal stimulation with light passing through a rotating polarizer [7,8]. Most POL-neurons are maximally excited at a particular E-vector orientation (Wmax) and are maximally inhibited at an orthogonal orientation, termed Wmin (polarization opponency)

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