Bart R. H. Geurten

Neural mechanisms underlying target detection in a dragonfly centrifugal neuron

SUMMARY Visual identification of targets is an important task for many animals searching for prey or conspecifics. Dragonflies utilize specialized optics in the dorsal acute zone, accompanied by higher-order visual neurons in the lobula complex, and descending neural pathways tuned to the motion of small targets. While recent studies describe the physiology of insect small target motion detector (STMD) neurons, little is known about the mechanisms that underlie their exquisite sensitivity to target motion. Lobula plate tangential cells (LPTCs), a group of neurons in dipteran flies selective for wide-field motion, have been shown to take input from local motion detectors consistent with the classic correlation model developed by Hassenstein and Reichardt in the 1950s. We have tested the hypothesis that similar mechanisms underlie the response of dragonfly STMDs. We show that an anatomically characterized centrifugal STMD neuron (CSTMD1) gives responses that depend strongly on target contrast, a clear prediction of the correlation model. Target stimuli are more complex in spatiotemporal terms than the sinusoidal grating patterns used to study LPTCs, so we used a correlation-based computer model to predict response tuning to velocity and width of moving targets. We show that increasing target width in the direction of travel causes a shift in response tuning to higher velocities, consistent with our model. Finally, we show how the morphology of CSTMD1 allows for impressive spatial interactions when more than one target is present in the visual field.

Sensory flow shaped by active sensing: sensorimotor strategies in electric fish

Summary Goal-directed behavior in most cases is composed of a sequential order of elementary motor patterns shaped by sensorimotor contingencies. The sensory information acquired thus is structured in both space and time. Here we review the role of motion during the generation of sensory flow focusing on how animals actively shape information by behavioral strategies. We use the well-studied examples of vision in insects and echolocation in bats to describe commonalities of sensory-related behavioral strategies across sensory systems, and evaluate what is currently known about comparable active sensing strategies in electroreception of electric fish. In this sensory system the sensors are dispersed across the animals body and the carrier source emitting energy used for sensing, the electric organ, is moved while the animal moves. Thus ego-motions strongly influence sensory dynamics. We present, for the first time, data of electric flow during natural probing behavior in Gnathonemus petersii (Mormyridae), which provide evidence for this influence. These data reveal a complex interdependency between the physical input to the receptors and the animals movements, posture and objects in its environment. Although research on spatiotemporal dynamics in electrolocation is still in its infancy, the emerging field of dynamical sensory systems analysis in electric fish is a promising approach to the study of the link between movement and acquisition of sensory information.

A Global In Vivo Drosophila RNAi Screen Identifies a Key Role of Ceramide Phosphoethanolamine for Glial Ensheathment of Axons

Glia are of vital importance for all complex nervous system. One of the many functions of glia is to insulate and provide trophic and metabolic support to axons. Here, using glial-specific RNAi knockdown in Drosophila, we silenced 6930 conserved genes in adult flies to identify essential genes and pathways. Among our screening hits, metabolic processes were highly represented, and genes involved in carbohydrate and lipid metabolic pathways appeared to be essential in glia. One critical pathway identified was de novo ceramide synthesis. Glial knockdown of lace, a subunit of the serine palmitoyltransferase associated with hereditary sensory and autonomic neuropathies in humans, resulted in ensheathment defects of peripheral nerves in Drosophila. A genetic dissection study combined with shotgun high-resolution mass spectrometry of lipids showed that levels of ceramide phosphoethanolamine are crucial for axonal ensheathment by glia. A detailed morphological and functional analysis demonstrated that the depletion of ceramide phosphoethanolamine resulted in axonal defasciculation, slowed spike propagation, and failure of wrapping glia to enwrap peripheral axons. Supplementing sphingosine into the diet rescued the neuropathy in flies. Thus, our RNAi study in Drosophila identifies a key role of ceramide phosphoethanolamine in wrapping of axons by glia.

Monogenic heritable autism gene neuroligin impacts Drosophila social behaviour

Autism spectrum disorders (ASDs) are characterized by deficits in social interactions, language development and repetitive behaviours. Multiple genes involved in the formation, specification and maintenance of synapses have been identified as risk factors for ASDs development. Among these are the neuroligin genes which code for postsynaptic cell adhesion molecules that induce the formation of presynapses, promote their maturation and modulate synaptic functions in both vertebrates and invertebrates. Neuroligin-deficient mice display abnormal social and vocal behaviours that resemble ASDs symptoms. Here we show for the fly Drosophila melanogaster that deletion of the dnl2 gene, coding for one of four Neuroligin isoforms, impairs social interactions, alters acoustic communication signals, and affects the transition between different behaviours. dnl2-Deficient flies maintain larger distances to conspecifics and males perform less female-directed courtship and male-directed aggressive behaviours while the patterns of these behaviours and general locomotor activity were not different from wild type controls. Since tests for olfactory, visual and auditory perception revealed no sensory impairments of dnl2-deficient mutants, reduced social interactions seem to result from altered excitability in central nervous neuropils that initiate social behaviours. Our results demonstrate that Neuroligins are phylogenetically conserved not only regarding their structure and direct function at the synapse but also concerning a shared implication in the regulation of social behaviours that dates back to common ancestors of humans and flies. In addition to previously described mouse models, Drosophila can thus be used to study the contribution of Neuroligins to synaptic function, social interactions and their implication in ASDs.

Saccadic body turns in walking Drosophila

Drosophila melanogaster structures its optic flow during flight by interspersing translational movements with abrupt body rotations. Whether these “body saccades” are accompanied by steering movements of the head is a matter of debate. By tracking single flies moving freely in an arena, we now discovered that walking Drosophila also perform saccades. Movement analysis revealed that the flies separate rotational from translational movements by quickly turning their bodies by 15 degrees within a tenth of a second. Although walking flies moved their heads by up to 20 degrees about their bodies, their heads moved with the bodies during saccadic turns. This saccadic strategy contrasts with the head saccades reported for e.g., blowflies and honeybees, presumably reflecting optical constraints: modeling revealed that head saccades as described for these latter insects would hardly affect the retinal input in Drosophila because of the lower acuity of its compound eye. The absence of head saccades in Drosophila was associated with the absence of haltere oscillations, which seem to guide head movements in other flies. In addition to adding new twists to Drosophila walking behavior, our analysis shows that Drosophila does not turn its head relative to its body when turning during walking.

Hearing regulates Drosophila aggression

Significance Behavior is regulated by information originating from different sensory modalities. Aggression is a universal social behavior with an important role in obtaining food, mates, territory, and social status. In this study, we demonstrate that hearing regulates aggression in Drosophila males. Further, we show that courtship and aggression songs differentially affect aggression, indicating that hearing contributes to the context-dependent regulation of aggression. Aggression is a universal social behavior important for the acquisition of food, mates, territory, and social status. Aggression in Drosophila is context-dependent and can thus be expected to involve inputs from multiple sensory modalities. Here, we use mechanical disruption and genetic approaches in Drosophila melanogaster to identify hearing as an important sensory modality in the context of intermale aggressive behavior. We demonstrate that neuronal silencing and targeted knockdown of hearing genes in the fly’s auditory organ elicit abnormal aggression. Further, we show that exposure to courtship or aggression song has opposite effects on aggression. Our data define the importance of hearing in the control of Drosophila intermale aggression and open perspectives to decipher how hearing and other sensory modalities are integrated at the neural circuit level.

Motor patterns during active electrosensory acquisition

Motor patterns displayed during active electrosensory acquisition of information seem to be an essential part of a sensory strategy by which weakly electric fish actively generate and shape sensory flow. These active sensing strategies are expected to adaptively optimize ongoing behavior with respect to either motor efficiency or sensory information gained. The tight link between the motor domain and sensory perception in active electrolocation make weakly electric fish like Gnathonemus petersii an ideal system for studying sensory-motor interactions in the form of active sensing strategies. Analyzing the movements and electric signals of solitary fish during unrestrained exploration of objects in the dark, we here present the first formal quantification of motor patterns used by fish during electrolocation. Based on a cluster analysis of the kinematic values we categorized the basic units of motion. These were then analyzed for their associative grouping to identify and extract short coherent chains of behavior. This enabled the description of sensory behavior on different levels of complexity: from single movements, over short behaviors to more complex behavioral sequences during which the kinematics alter between different behaviors. We present detailed data for three classified patterns and provide evidence that these can be considered as motor components of active sensing strategies. In accordance with the idea of active sensing strategies, we found categorical motor patterns to be modified by the sensory context. In addition these motor patterns were linked with changes in the temporal sampling in form of differing electric organ discharge frequencies and differing spatial distributions. The ability to detect such strategies quantitatively will allow future research to investigate the impact of such behaviors on sensing.

Neuroprotection and endocytosis: erythropoietin receptors in insect nervous systems

Erythropoietin (Epo) plays a dual role as an erythropoiesis‐stimulating hormone and a locally produced cytoprotectant in various vertebrate tissues. Splice variants and engineered derivatives of Epo that mediate neuroprotection but do not stimulate erythropoiesis suggest that alternative receptors, different from the ‘classical’ homodimeric receptor involved in haematopoiesis, mediate neuroprotective Epo functions. Previous studies on grasshoppers demonstrated neuroprotective and neuroregenerative effects of Epo that involved similar transduction pathways as in mammals. To advance the characterization of yet unidentified neuroprotective Epo receptors, we studied the neuroprotective potency of the human non‐erythropoietic Epo splice variant EV‐3 in primary cultured locust brain neurons. We demonstrate that EV‐3, like Epo, protects locust neurons from hypoxia‐induced apoptotic death through activation of the Janus kinase/signal transducer and activator of transcription transduction pathway. Using the fluorescent dye FM1–43 to quantify endocytotic activity we show that both Epo and EV‐3 increase the number of fluorescently labelled endocytotic vesicles. This reveals that binding of Epo to its neuroprotective receptor induces endocytosis, as it has been described for the mammalian homodimeric Epo‐receptor expressed by erythroid progenitors. Reduction in Epo‐stimulated endocytotic activity following pre‐exposure to EV‐3 indicated that both Epo and its splice variant bind to the same receptor on locust neurons. The shared neuroprotective potency of Epo and EV‐3 in insect and mammalian neurons, in the absence of erythropoietic effects of EV‐3 in mammals, suggests a greater similarity of the unidentified nervous Epo receptors (or receptor complexes) across phyla than between mammalian haematopoietic and neuroprotective receptors. Insects may serve as suitable models to evaluate the specific protective mechanisms mediated by Epo and its variants in non‐erythropoietic mammalian tissues.

Saccadic Movement Strategy in Common Cuttlefish (Sepia officinalis)

Most moving animals segregate their locomotion trajectories in short burst like rotations and prolonged translations, to enhance distance information from optic flow, as only translational, but not rotational optic flow holds distance information. Underwater, optic flow is a valuable source of information as it is in the terrestrial habitat, however, so far, it has gained only little attention. To extend the knowledge on underwater optic flow perception and use, we filmed the movement pattern of six common cuttlefish (Sepia officinalis) with a high speed camera in this study. In the subsequent analysis, the center of mass of the cuttlefish body was manually traced to gain thrust, slip, and yaw of the cuttlefish movements over time. Cuttlefish indeed performed short rotations, saccades, with rotational velocities up to 343°/s. They clearly separated rotations from translations in line with the saccadic movement strategy documented for animals inhabiting the terrestrial habitat as well as for the semiaquatic harbor seals before. However, this separation only occurred during fin motion. In contrast, during jet propelled swimming, the separation between rotational and translational movements and thus probably distance estimation on the basis of the optic flow field is abolished in favor of high movement velocities. In conclusion, this study provides first evidence that an aquatic invertebrate, the cuttlefish, adopts a saccadic movement strategy depending on the behavioral context that could enhance the information gained from optic flow.

Sound Communication in Drosophila

The fruit fly Drosophila melanogaster communicates acoustically via courtship songs and hears with antennal ears. Research over the past decade has provided insights into the neuronal basis of Drosophila sound production and hearing and the functional workings of Drosophila ears: the neural substrate for song production has been narrowed down to subsets of FruitlessM positive neurons, and the neural pathways for hearing have begun to be revealed. Mechanisms of sound transduction, adaptation, and amplification in the fruit fly’s ear have been uncovered, and auditory relevant molecules have emerged from mutant screens. This chapter summarized the current state of research on Drosophila sound communication and hearing and discusses recent progress in the field.