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Donlea, J. M.

Publications and source records attributed to Donlea, J. M..

6 recordsLinked to original sources

Developmental sleep reallocation enables metabolic adaptation in desert flies

Sleep is essential for adaptation and survival across the lifespan, yet the ecological pressures shaping sleep ontogeny remain poorly understood. We investigated sleep across early developmental stages in Drosophila mojavensis, a stress-resilient desert-adapted species. While adult D.mojavensis exhibit prolonged and consolidated sleep, along with enhanced starvation tolerance and survival compared to Drosophila melanogaster, the developmental trajectory underlying these adaptation strategies for surviving in harsh environments is unknown. Moreover, during developmental (larval) periods, animals do not encounter the same environmental stressors experienced by adults (e.g., food scarcity, extreme temperatures). We find that in contrast to adults, D.mojavensis larvae exhibit reduced and fragmented sleep relative to D.melanogaster. D.mojavensis larval sleep is also deeper, reflecting a shift toward increased sleep efficiency rather than simple sleep loss. D.mojavensis larvae consume more food than D.melanogaster and survive longer under starvation, suggesting a strategic tradeoff by suppressing sleep to prioritize nutrient intake and energy storage early in life while resources are more abundant. Metabolic analyses reveal elevated triglyceride accumulation in D.mojavensis across their lifespan, indicating enhanced energy storage capacity. These findings provide an example of how, within a fixed genetic background, an animal can reallocate sleep in opposing manners to maximize survival and energetics depending upon ecological pressures unique to each phase of life.

neuroscience↗

Breaking free from the clocks tyranny restores memory to brain damaged flies

The relationship between sleep and memory is an active topic of investigation. In this context, we demonstrate that enhancing sleep restores memory to flies with ablated Mushroom Bodies (MB), a key memory center; this is consistent across several memory assays. Mapping the underlying circuitry reveals circadian modulation of a subset of Dopaminergic neurons (DANs) that modulate aversive learning. Using imaging, we show that MB-ablation disrupts, and sleep restores the time of day these neurons are most responsive. Knocking down the receptor for the clock output signal, Pigment-dispersing factor (Pdfr), in this subset of DANs restores memory to MB-ablated flies. Crucially, MB-ablation does not result in memory impairments in the absence of a functioning clock. Our results reveal neuromodulations key role in cognitive restoration, where sleep aids memory in damaged brains, but a functioning clock unexpectedly hinders this process.

neuroscience↗

Elevated sleep need in a stress-resilient Drosophila species

Sleep is broadly conserved across the animal kingdom, but can vary widely between species. It is currently unclear which types of selective pressures and sleep regulatory mechanisms influence differences in sleep between species. The fruit fly Drosophila melanogaster has become a successful model system for examining sleep regulation and function, but little is known about the sleep patterns and need for sleep in many related fly species. Here, we find that Drosophila mojavensis, a fly species that has adapted to extreme desert environments, exhibits strong increases in sleep compared to D. melanogaster. Long-sleeping D. mojavensis show intact sleep homeostasis, indicating that these flies carry an elevated need for sleep. In addition, D. mojavensis exhibit altered abundance or distribution of several sleep/wake related neuromodulators and neuropeptides that are consistent with their reduced locomotor activity, and increased sleep. Finally, we find that in a nutrient-deprived environment, the sleep responses of individual D. mojavensis are correlated with their survival time. Our results demonstrate that D. mojavensis is a novel model for studying organisms with high sleep need, and for exploring sleep strategies that provide resilience in extreme environments.

neuroscience↗

Mutation of the Drosophila serotonin transporter dSERT disrupts courtship and feeding and increases both daytime and nighttime sleep

The Serotonin Transporter (SERT) regulates extracellular serotonin levels and is the target of most current drugs used to treat depression. The mechanisms by which inhibition of SERT activity influences behavior are poorly understood. To address this question in the model organism Drosophila melanogaster, we developed new loss of function mutations in Drosophila SERT (dSERT). Previous studies in both flies and mammals have implicated serotonin as an important neuromodulator of sleep, and our newly generated dSERT mutants show an increase in total sleep and altered sleep architecture. Differences in daytime vs. nighttime sleep architecture as well as genetic rescue experiments unexpectedly suggest that distinct serotonergic circuits may modulate daytime versus nighttime sleep. dSERT mutants also show defects in copulation and food intake, akin to the clinical side effects of SSRIs. Starvation did not overcome the sleep drive in the mutants. Additionally in males, but not female dSERT mutants, the drive to mate also failed to overcome sleep drive. dSERT may be used to further explore the mechanisms by which serotonin regulates sleep and its interplay with other complex behaviors. Author SummaryMany medications used to treat depression and anxiety act by changing serotonin levels in the brain. Fruit flies also use serotonin and can be used as a model to study the brain. We have made a fly mutant for the serotonin transporter (SERT), which is the target of antidepressants in humans. The mutants sleep more, eat less, and have a decreased sex drive. These flies can be used to study the neuronal pathways by which serotonin regulates sleep, eating and sexual behaviors and may help us to understand the behavioral effects of antidepressants.

neuroscience↗

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.

neuroscience↗

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↗