Processing of sky compass signals at different stages of the polarization-vision pathway in the brain of the desert locust (Schistocerca gregaria)

Obwohl Insekten ein relativ kleines Gehirn aufweisen, zeigen sie außergewöhnliche Leistungen in räumlicher Orientierung und Navigation. Während langer Wanderflüge oder der Rückkehr zu einem Nestplatz können sie die ideale Route bestimmen und verfolgen, die sie auf kürzestem und schnellstem Weg zu ihrem Ziel führt. Hierbei können vor allem Kompasssignale des Himmels eine erhebliche Rolle spielen. Neben der Sonne, dem hellsten Punkt am Himmel, liefern weitere Himmelssignale wie der Farbgradient oder das Polarisationsmuster des Himmels Möglichkeiten zur Orientierung. Beide Himmelserscheinungen entstehen als Resultat der Streuung von Sonnenlicht an atmosphärischen Partikeln und bilden präzise Referenzen am Himmel. Verhaltensversuche haben gezeigt, dass Wüstenheuschrecken der Gattung Schistocerca gregaria während ihren langen Wanderungen über Nordafrika und Ostasien linear polarisiertes Licht des Himmels zur Navigation nutzen können. Hierfür verfügen sie über eine spezialisierte Augenregion zur Detektion von polarisiertem Licht, die sich dorsal am Komplexauge morphologisch vom restlichen Auge hervorhebt und als dorsale Randregion bezeichnet wird. Angesichts ihres relativ großen Gehirnes und der damit einhergehenden guten physiologischen Zugänglichkeit hat sich die Wüstenheuschrecke Schistocerca gregaria als hervorragendes Modellobjekt erwiesen, um die neuronalen Prinzipien der Verarbeitung von polarisiertem Licht im Insektengehirn zu erforschen. Die Prozessierung von Polarisationssignalen findet in sukzessiv angeordneten Gehirnarealen der Heuschrecke statt, die die sogenannte Polarisationssehbahn bilden. Die Axone der Fotorezeptoren in der dorsalen Randregion ziehen aus dem Auge in zwei distinkte, ebenfalls dorsal lokalisierte Randregionen der optischen Neuropile Lamina und Medulla. Über Transmedulla-Neurone – auch als „Line Tangential“-Neurone bezeichnet – ist die dorsale Randregion der Medulla mit einem Bereich im Zentralhirn verbunden, der als anteriorer optischer Tuberkel bezeichnet wird. Die Polarisationsinformation wird dann zu den nächsten Stationen der Polarisationssehbahn, der medianen Olive und dem lateralen Dreieck geleitet. Hier transferieren Neurone die Polarisationssignale auf Eingangsneurone des Zentralkomplexes. Der Zentralkomplex ist das zentrale Prozessierungsareal für polarisiertes Licht und erfüllt möglicherweise eine Rolle als interner Kompass im Heuschreckengehirn, in dem die räumliche Orientierung des Tieres relativ zum solaren Meridian kodiert wird. Ausgangsneurone des Zentralkomplexes könnten die Polarisationssignale auf absteigende Neurone übertragen, deren Axone wiederum zu den Kontrollzentren in den Thorakalganglien projizieren. Um die Kombination der Polarisationsinformation mit weiteren visuellen Reizen zu untersuchen, und um einen tieferen Einblick in Vorgänge der Zeitkompensation und Modulation des Polarisationsnetzwerks zu gewinnen, wurden in dieser Arbeit elektrophysiologische und anatomische Untersuchungen polarisationssensitiver Neurone durchgeführt

3D-Reconstructions and Virtual 4D-Visualization to Study Metamorphic Brain Development in the Sphinx Moth Manduca Sexta

During metamorphosis, the transition from the larva to the adult, the insect brain undergoes considerable remodeling: new neurons are integrated while larval neurons are remodeled or eliminated. One well acknowledged model to study metamorphic brain development is the sphinx moth Manduca sexta. To further understand mechanisms involved in the metamorphic transition of the brain we generated a 3D standard brain based on selected brain areas of adult females and 3D reconstructed the same areas during defined stages of pupal development. Selected brain areas include for example mushroom bodies, central complex, antennal- and optic lobes. With this approach we eventually want to quantify developmental changes in neuropilar architecture, but also quantify changes in the neuronal complement and monitor the development of selected neuronal populations. Furthermore, we used a modeling software (Cinema 4D) to create a virtual 4D brain, morphing through its developmental stages. Thus the didactical advantages of 3D visualization are expanded to better comprehend complex processes of neuropil formation and remodeling during development. To obtain datasets of the M. sexta brain areas, we stained whole brains with an antiserum against the synaptic vesicle protein synapsin. Such labeled brains were then scanned with a confocal laser scanning microscope and selected neuropils were reconstructed with the 3D software AMIRA 4.1

Dung beetles use their dung ball as a mobile thermal refuge

At midday, surface temperatures in the desert often exceed 60°C. To be active at this time, animals need extraordinary behavioural or physiological adaptations. Desert ants, for instance, spend up to 75% of their foraging time cooling down on elevated thermal refuges such as grass stalks [1]. Ball-rolling dung beetles work under similar thermal conditions in South African savannahs. After landing at a fresh dung pile, a beetle quickly forms a dung ball and rolls it away in a straight line, head down, walking backwards [2]. Earlier studies have shown that some dung beetles maintain an elevated body temperature to gain a competitive advantage [3], [4] and [5], and that heat shunting may prevent overheating during flight [6] and [7]. However, we know little about the behavioural strategies beetles might employ to mitigate heat stress while rolling their dung balls. Using infrared thermography and behavioural experiments, we show here that dung beetles use their dung ball as a mobile thermal refuge onto which they climb to cool down while rolling across hot soil. We further demonstrate that the moist ball functions not only as a portable platform, but also as a heat sink, which effectively cools the beetle as it rolls or climbs onto it

The Locust Standard Brain: A 3D Standard of the Central Complex as a Platform for Neural Network Analysis

Many insects use the pattern of polarized light in the sky for spatial orientation and navigation. We have investigated the polarization vision system in the desert locust. To create a common platform for anatomical studies on polarization vision pathways, Kurylas et al. (2008) have generated a three-dimensional (3D) standard brain from confocal microscopy image stacks of 10 male brains, using two different standardization methods, the Iterative Shape Averaging (ISA) procedure and the Virtual Insect Brain (VIB) protocol. Comparison of both standardization methods showed that the VIB standard is ideal for comparative volume analysis of neuropils, whereas the ISA standard is the method of choice to analyze the morphology and connectivity of neurons. The central complex is a key processing stage for polarization information in the locust brain. To investigate neuronal connections between diverse central-complex neurons, we generated a higher-resolution standard atlas of the central complex and surrounding areas, using the ISA method based on brain sections from 20 individual central complexes. To explore the usefulness of this atlas, two central-complex neurons, a polarization-sensitive columnar neuron (type CPU1a) and a tangential neuron that is activated during flight, the giant fan-shaped (GFS) neuron, were reconstructed 3D from brain sections. To examine whether the GFS neuron is a candidate to contribute to synaptic input to the CPU1a neuron, we registered both neurons into the standardized central complex. Visualization of both neurons revealed a potential connection of the CPU1a and GFS neurons in layer II of the upper division of the central body

Night sky orientation with diurnal and nocturnal eyes: dim-light adaptations are critical when the moon is out of sight

The visual systems of many animals feature energetically costly specializations to enable them to function in dim light. It is often unclear, however, how large the behavioural benefit of these specializations is, because a direct comparison in a behaviourally relevant task between closely related day- and night-active species is not usually possible. Here we compared the orientation performance of diurnal and nocturnal species of dung beetles, Scarabaeus (Kheper) lamarcki and Scarabaeus satyrus, respectively, attempting to roll dung balls along straight paths both during the day and at night. Using video tracking, we quantified the straightness of paths and the repeatability of roll bearings as beetles exited a flat arena in their natural habitat or under controlled conditions indoors. Both species oriented equally well when either the moon or an artificial point light source was available, but when the view of the moon was blocked and only wide-field cues such as the lunar polarization pattern or the stars were available for orientation, nocturnal beetles were oriented substantially better. We found no evidence that ball-rolling speed changed with light level, which suggests little or no temporal summation in the visual system. Finally, we found that both diurnal and nocturnal beetles tended to choose bearings that led them towards a bright light source, but away from a dim one. Our results show that even diurnal insects, at least those with superposition eyes, could orient by the light of the moon, but that dim-light adaptations are needed for precise orientation when the moon is not visible

3D Standard Brain of the Red Flour Beetle Tribolium Castaneum: A Tool to Study Metamorphic Development and Adult Plasticity

The red flour beetle Tribolium castaneum is emerging as a further standard insect model beside Drosophila. Its genome is fully sequenced and it is susceptible for genetic manipulations including RNA-interference. We use this beetle to study adult brain development and plasticity primarily with respect to the olfactory system. In the current study, we provide 3D standard brain atlases of freshly eclosed adult female and male beetles (A0). The atlases include eight paired and three unpaired neuropils including antennal lobes (ALs), optic lobe neuropils, mushroom body calyces and pedunculi, and central complex. For each of the two standard brains, we averaged brain areas of 20 individual brains. Additionally, we characterized eight selected olfactory glomeruli from 10 A0 female and male beetles respectively, which we could unequivocally recognize from individual to individual owing to their size and typical position in the ALs. In summary, comparison of the averaged neuropil volumes revealed no sexual dimorphism in any of the reconstructed neuropils in A0 Tribolium brains. Both, the female and male 3D standard brain are also used for interspecies comparisons, and, importantly, will serve as future volumetric references after genetical manipulation especially regarding metamorphic development and adult plasticity

A unified platform to manage, share, and archive morphological and functional data in insect neuroscience

Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction are findable, accessible and reusable. To promote an open data culture, we have therefore developed the InsectBrainDatabase (IBdb), a free online platform for insect neuroanatomical and functional data. The IBdb facilitates biological insight by enabling effective cross-species comparisons, by linking neural structure with function, and by serving as general information hub for insect neuroscience. The IBdb allows users to not only effectively locate and visualize data, but to make them widely available for easy, automated reuse via an application programming interface. A unique private mode of the database expands the IBdb functionality beyond public data deposition, additionally providing the means for managing, visualizing, and sharing of unpublished data. This dual function creates an incentive for data contribution early in data management workflows and eliminates the additional effort normally associated with publicly depositing research data

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

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

The Dung Beetle Compass

What do a burly rower, a backstroke swimmer and a hard-working South African dung beetle all have in common? The answer is: they all benefit from moving along a straight path, and do so moving backwards. This, however, is where the similarity ends. While the rower has solved this navigational challenge by handing the task of steering to the coxswain, who faces the direction of travel, and the swimmer is guided down her lane by colourful ropes, the beetle puts its faith in the sky. From here, it utilises a larger repertoire of celestial compass cues than is known to be used by any other animal studied to date. A robust internal compass, designed to interpret directional information, has evolved under the selective pressure of shifting today's lunch efficiently out of reach of competitors, also drawn to the common buffet. While this is a goal that beetles might share with the hungry athletes, they reach it with drastically different brain powers; the brain of the beetle is several times smaller than a match head, containing fewer than a million neurons. In this Primer, Marie Dacke and Basil el Jundi examine the behavioural and neuronal mechanisms of the dung beetle's celestial compass underlying straight-line orientation

Insect Orientation : The Drosophila Wind Compass Pathway

Wind can act as an external cue to control an animal's heading. A new study reveals the neural mechanisms behind the wind information pathway in the insect brain