Processing of Polarization Patterns and Visual Self-Motion in the Locust Central Complex for Spatial Orientation

Despite their relatively small brains with comparatively low neuron counts, insects show complex navigation behavior such as seasonal long-range migration, path integration, and precise straight-line movement. Spatial navigation requires a sense of current heading, which must be tethered to prominent external cues and updated by internal cues that result from movement. Global external cues such as the position of the sun may provide a reference frame for orientation. Sunlight is polarized by scattering in the atmosphere, which results in a sky-spanning polarization pattern that directly depends on the current solar position and makes polarization information, like the sun itself, useful as an external reference cue. Internally, moving through the environment generates optic flow---the motion of the viewed scenery on the retina---, which may inform about turning maneuvers, movement speed, and covered distance. Many insects use these external and internal cues for orientation, and the neuronal center for spatial navigation likely is the central complex, a higher-order brain structure where sensory information is integrated to form an internal compass representation of the current heading. This thesis addresses the question how celestial compass cues, specifically the polarization pattern, and optic flow are processed in the central complex of the desert locust, a long-range migratory insect. All chapters except the last one are electrophysiological studies in which single central-complex neurons were intracellularly recorded while presenting visual stimuli. The neurons' anatomy was histologically determined by dye injection in order to infer their role in the neural network. The studies in Chapters 1 and 2 show that the central complex contains a neuronal compass that robustly signals the sun direction based on direct sunlight and the integration of the whole solar polarization pattern. This shows that the locust brain uses all available skylight cues in order to form a unified compass signal, enabling robust navigation under different environmental conditions. The study in Chapter 3 further examines how neurons at the input stage of the central complex process skylight cues. Already at this stage, single neurons integrate visual information from large areas of the sky and have receptive fields suitable to build the skylight compass. Chapter 4 sheds light on the detection sensitivity for the angle of polarization, finding that central-complex neurons are highly sensitive in this regard, adapted to analyze the skylight polarization pattern almost in its entirety and under unfavorable environmental conditions. In Chapter 5 the locust central complex was scanned for neurons that receive optic flow information. Neurons at virtually all network stages are sensitive to optic flow, mainly uncoupled from skylight-cue sensitivity. This highlights that sensory information is flexibly processed in the central complex, presumably depending on the animal's current behavioral demands. Further, the study hypothesizes how horizontal turning motion is processed in order to update the internal heading representation, backed up by a computational model that adheres to brain anatomy and physiological data. Altogether, these studies advance the understanding of how external and internal cues are processed in the central-complex network in order to establish a sense of orientation in the insect brain. Finally, I contributed with data sets and programming code to the development of the InsectBrainDatabase (www.insectbraindb.org), a free online database tool designed to manage, share and publish anatomical and functional research data (Chapter 6)

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

Integration of optic flow into the sky compass network in the brain of the desert locust

Flexible orientation through any environment requires a sense of current relative heading that is updated based on self-motion. Global external cues originating from the sky or the earth‘s magnetic field and local cues provide a reference frame for the sense of direction. Locally, optic flow may inform about turning maneuvers, travel speed and covered distance. The central complex in the insect brain is associated with orientation behavior and largely acts as a navigation center. Visual information from global celestial cues and local landmarks are integrated in the central complex to form an internal representation of current heading. However, it is less clear how optic flow is integrated into the central-complex network. We recorded intracellularly from neurons in the locust central complex while presenting lateral grating patterns that simulated translational and rotational motion to identify these sites of integration. Certain types of central-complex neurons were sensitive to optic-flow stimulation independent of the type and direction of simulated motion. Columnar neurons innervating the noduli, paired central-complex substructures, were tuned to the direction of simulated horizontal turns. Modeling the connectivity of these neurons with a system of proposed compass neurons can account for rotation-direction specific shifts in the activity profile in the central complex corresponding to turn direction. Our model is similar but not identical to the mechanisms proposed for angular velocity integration in the navigation compass of the fly Drosophila

A Model for Optic Flow Integration in Locust Central-Complex Neurons Tuned to Head Direction

Navigation is a fundamental cognitive function of virtually all moving animals. Several navigation strategies require an estimate of the current travelling direction that is updated continuously. In the central complex of the insect brain, multimodal cues are fused into a compass-like head direction representation. Based on the proposed connectivity of columnar neurons in the central complex of the desert locust we designed a computational model to examine how these neurons could maintain a stable representation of heading direction and how shifts occur by optic flow signals when the animal turns. Our proposed model architecture shows that the activity of head direction-encoding CL1a neurons remains stable if the activity of a second class of columnar neurons, CL2, is exactly the same. Shifts occur via modulation of the network connectivity. Our model can be used to deduce testable hypotheses where data are lacking, inspiring new avenues of experimental investigations

InsectBrainDatabase - A unified platform to manage, share, and archive morphological and functional data

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