Biology subjects

Omoto, J. J.

Publications and source records attributed to Omoto, J. J..

7 recordsLinked to original sources

bioRxiv2026

Flies evolved a gyrocompass to maintain navigational accuracy during rapid flight maneuvers

Halteres, the miniaturized hindwings of flies, function as biological gyroscopes that encode angular velocity during flight. Although their established role is to detect flight perturbations and trigger compensatory manoeuvers, here we show that halteres also function as a gyrocompass, maintaining an accurate estimate of heading during rapid turns. To overcome the incompatibility between rapid body rotations and two-photon imaging, we exploited the physics of haltere mechano-transduction to reproduce the inertial forces acting on the halteres during rapid body rotations using micron-scale oscillations of the thorax. Our experiments demonstrate that flies update their internal compass during rapid turns by integrating inertial measurements with predictions derived from efference copy signals. Because body saccades exceed the temporal bandwidth of visual motion processing, this inertial computation allows flies to maintain an accurate internal compass throughout these rapid manoeuvres. This capability may enable flies to compute critical parameters such as wind direction and ground speed by comparing measurements made before and after each saccade. Our findings suggest that an ancestral flight-stabilization system was evolutionarily co-opted into a biological gyrocompass, a new function that may have contributed to the adaptive radiation of flies.

neuroscience↗

bioRxiv2023

Descending control and regulation of spontaneous flight turns in Drosophila

The clumped distribution of resources in the world has influenced the pattern of foraging behavior since the origins of life, selecting for a common locomotor search motif in which straight movements through resource-poor regions alternate with zig-zag exploration in resource-rich domains (Berg, 2000). For example, flies execute rapid changes in flight heading called body saccades during local search (Censi et al., 2013; Collett and Land, 1975; Schilstra and van Hateren, 1999; Wagner and Land, 1986), but suppress these turns during long-distance dispersal (Giraldo et al., 2018; Leitch et al., 2021) or when surging upwind after encountering an attractive odor plume (Budick and Dickinson, 2006; van Breugel and Dickinson, 2014). Here, we describe the key cellular components of a neural network in flies that generates spontaneous turns as well as a specialized neuron that inhibits the network to promote straight flight. Using 2-photon imaging, optogenetic activation, and genetic ablation, we show that only four descending neurons appear sufficient to generate the descending commands to execute flight saccades. The network is organized into two functional couplets--one for right turns and one for left--with each couplet consisting of an excitatory (DNae014) and inhibitory (DNb01) neuron that project to the flight motor neuropil within the ventral nerve cord. Using resources from recently published connectomes of the fly brain (Scheffer et al., 2020; Dorkenwald et al., 2023; Schlegel et al., 2023), we identified a large, unique interneuron (VES041) that forms inhibitory connections to all four saccade command neurons and created specific genetic driver lines for this cell. As predicted by its connectivity, activation of VES041 strongly suppresses saccades, suggesting that it regulates the transition between local search and long-distance dispersal. These results thus identify the critical elements of a network that not only structures the locomotor behavior of flies, but may also play a crucial role in their foraging ecology.

neuroscience↗

bioRxiv2022

The role of a population of descending neurons in the optomotor response in flying Drosophila

To maintain stable flight, animals continuously perform trimming adjustments to compensate for internal and external perturbations. Whereas animals use many different sensory modalities to detect such perturbations, insects rely extensively on optic flow to modify their motor output and remain on course. We studied this behavior in the fruit fly, Drosophila melanogaster, by exploiting the optomotor response, a robust reflex in which an animal steers so as to minimize the magnitude of rotatory optic flow it perceives. Whereas the behavioral and algorithmic structure of the optomotor response has been studied in great detail, its neural implementation is not well-understood. In this paper, we present findings implicating a group of nearly homomorphic descending neurons, the DNg02s, as a core component for the optomotor response in flying Drosophila. Prior work on these cells suggested that they regulate the mechanical power to the flight system, presumably via connections to asynchronous flight motor neurons in the ventral nerve cord. When we chronically inactivated these cells, we observed that the magnitude of the optomotor response was diminished in proportion to the number of cells silenced, suggesting that the cells also regulate bilaterally asymmetric steering responses via population coding. During an optomotor response, flies coordinate changes in wing motion with movements of their head, abdomen, and hind legs, which are also diminished when the DNg02 cells are silenced. Using two-photon functional imaging, we show that the DNg02 cells respond most strongly to patterns of horizontal motion and that neuronal activity is closely correlated to motor output. However, unilateral optogenetic activation of DNg02 neurons does not elicit the asymmetric changes in wing motion characteristic of the optomotor response to a visual stimulus, but rather generates bilaterally symmetric increases in wingbeat amplitude. We interpret our experiments to suggest that flight maneuvers in flies require a more nuanced coordination of power muscles and steering muscles than previously appreciated, and that the physical flight apparatus of a fly might permit mechanical power to be distributed differentially between the two wings. Thus, whereas our experiments identify the DNg02 cells as a critical component of the optomotor reflex, our results suggest that other classes of descending cells targeting the steering muscle motor neurons are also required for the behavior.

neuroscience↗

bioRxiv2021

Opposing subclasses of Drosophila ellipsoid body neurons promote and suppress sleep

Recent work in Drosophila has uncovered several neighboring classes of sleep-regulatory neurons within the central complex. However, the logic of connectivity and network motifs remains limited by the incomplete examination of relevant cell types. Using a recent genetic-anatomical classification of ellipsoid body ring neurons, we conducted a thermogenetic screen to assess sleep/wake behavior and discovered two opposing populations: sleep-promoting R3m and wake-promoting R3d neurons. Activation of these neurons influences sleep duration and architecture by prolonging or shortening sleep bouts, suggesting a key role in sleep maintenance. R3m and R3d neurons are GABAergic and require GABA synthesis for their effects on sleep. Finally, we use a fluorescent reporter for putative synaptic partners to embed these neurons within the known sleep-regulatory network; R3m and R3d neurons lay downstream of wake-active Helicon cells, and R3m neurons likely inhibit R3d neurons. Together, the data presented herein suggest a neural mechanism by which previously uncharacterized circuit elements operate within the sleep homeostat to stabilize sleep-wake states.

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bioRxiv2020

A visual pathway for skylight polarization processing in Drosophila

Many insects use patterns of polarized light in the sky to orient and navigate. Here we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the flys sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the sky compass pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

neuroscience↗

bioRxiv2018

Neuronal constituents and putative interactions within the Drosophila ellipsoid body neuropil

The central complex (CX) is a midline-situated collection of neuropil compartments in the arthropod central brain, implicated in higher-order processes such as goal-directed navigation. Here, we provide a systematic genetic-neuroanatomical analysis of the ellipsoid body (EB), a compartment which represents a major afferent portal of the Drosophila CX. The neuropil volume of the EB, along with its prominent input compartment, called the bulb, is subdivided into precisely tessellated domains, distinguishable based on intensity of the global marker DN-cadherin. EB tangential elements (so-called ring neurons), most of which are derived from the DALv2 neuroblast lineage, interconnect the bulb and EB domains in a topographically-organized fashion. Using the DN-cadherin domains as a framework, we first characterized the bulb-EB connectivity by Gal4 driver lines expressed in different DALv2 ring neuron (R-neuron) subclasses. We identified 11 subclasses, 6 of which correspond to previously described projection patterns, and 5 novel patterns. These subclasses both spatially (based on EB innervation pattern) and numerically (cell counts) summate to the total EB volume and R-neuron cell number, suggesting that our compilation of R-neuron subclasses approaches completion. EB columnar elements, as well as non-DALv2 derived extrinsic ring neurons (ExR-neurons), were also incorporated into this anatomical framework. Finally, we addressed the connectivity between R-neurons and their targets, using the anterograde trans-synaptic labeling method, trans-Tango. This study demonstrates putative interactions of R-neuron subclasses and reveals general principles of information flow within the EB network. Our work will facilitate the generation and testing of hypotheses regarding circuit interactions within the EB and the rest of the CX.

neuroscience↗

bioRxiv2018

Developmentally arrested precursors of pontine neurons establish an embryonic blueprint of the Drosophila central complex

Serial electron microscopic analysis shows that the Drosophila brain at hatching possesses a large fraction of developmentally arrested neurons with a small soma, heterochromatin-rich nucleus, and unbranched axon lacking synapses. We digitally reconstructed all 812 \" small undifferentiated\" (SU) neurons on both hemispheres and assigned them to the known brain lineages. 54 SU neurons belonging to the DM1-4 lineages, which generate all columnar neurons of the central complex, form an embryonic nucleus of the fan-shaped body (FB). These \" FB pioneers\" develop into a speci1c class of bi-columnar elements, the pontine neurons. Even though later born, unicolumnar DM1-4 neurons fasciculate with the FB pioneers, selective ablation of these cells did not result in gross abnormalities of the trajectories of unicolumnar neurons, indicating that axonal path1nding of the two systems is controlled independently. Our comprehensive spatial and developmental analysis of the SU neuron adds to our understanding of the establishment of neuronal circuitry.

neuroscience↗