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Simpson, J. H.

Publications and source records attributed to Simpson, J. H..

6 recordsLinked to original sources

Behavior choices amongst grooming, feeding, and courting in Drosophila show contextual flexibility, not an absolute hierarchy of needs

To determine the algorithmic rules and neural circuits controlling selection amongst competing behaviors, we established assays where adult Drosophila melanogaster choose between grooming and feeding, grooming and courting, or feeding and courting. We find that there is not an absolute hierarchy: while flies typically perform grooming first, they can choose to feed if sufficiently starved, or court if an appropriate female is available. Flies alternate between competing behaviors, performing short bouts of each action rather than completely satisfying one drive before transitioning to another. While we did not do an exhaustive screen, from the candidates we examined, we did not find evidence for a specific genetic or neuronal locus that affects all decisions. We did identify genetic background effects, suggesting that multiple genes may contribute to decision-making priorities. Our results add to a growing body of work on decision-making in Drosophila and provide a foundation for future investigation of the exact neural circuits required to achieve appropriate choices. Summary StatementFlies alternate between competing behaviors. The choice amongst positive actions depends on context and relative drive levels. No central decision-making locus was identified.

animal behavior and cognition↗

Inhibitory circuits coordinate leg movements during Drosophila grooming

Limbs execute diverse actions coordinated by the nervous system through multiple motor programs. The basic architecture of motor neurons that activate muscles which articulate joints for antagonistic flexion and extension movements is conserved from flies to vertebrates. While excitatory premotor circuits are expected to establish sets of leg motor neurons that work together, our study uncovered an instructive role for inhibitory circuits -- including their ability to generate rhythmic leg movements. Using electron microscopy data in the Drosophila nerve cord, we categorized [~]120 GABAergic inhibitory neurons from the 13A and 13B hemilineages into classes based on similarities in morphology and connectivity. By mapping their connections, we uncovered pathways for inhibiting specific groups of motor neurons, disinhibiting antagonistic counterparts, and inducing alternation between flexion and extension. We tested the function of specific inhibitory neurons through optogenetic activation and silencing, using high resolution quantitative analysis of leg movements during grooming. We combined findings from anatomical and behavioral analyses to construct a computational model that can reproduce major aspects of the observed behavior, demonstrating that these premotor inhibitory circuits can generate rhythmic leg movements. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=199 SRC="FIGDIR/small/597468v5_ufig1.gif" ALT="Figure 1"> View larger version (53K): org.highwire.dtl.DTLVardef@1d75349org.highwire.dtl.DTLVardef@19ce5bforg.highwire.dtl.DTLVardef@1af5f6corg.highwire.dtl.DTLVardef@a1de95_HPS_FORMAT_FIGEXP M_FIG C_FIG

neuroscience↗

Mechanosensory and command contributions to the Drosophila grooming sequence

Flies groom in response to competing mechanosensory cues in an anterior to posterior order using specific legs. From behavior screens, we identified a pair of cholinergic command-like neurons, Mago-no-Te (MGT), whose optogenetic activation elicits thoracic grooming by hind legs. Thoracic grooming is typically composed of body sweeps and leg rubs in alternation, but clonal analysis coupled with amputation experiments revealed that MGT activation only commands the body sweeps: initiation of leg rubbing requires contact between leg and thorax. With new electron microscopy (EM) connectome data for the ventral nerve cord (VNC), we uncovered a circuit-based explanation for why stimulation of posterior thoracic mechanosensory bristles initiates cleaning by the hind legs. Our previous work showed that flies weigh mechanosensory inputs across the body to select which part to groom, but we did not know why the thorax was always cleaned last. Here, the connectome for the VNC enabled us to identify a pair of GABAergic inhibitory neurons, UMGT1, that receive diverse sensory inputs and synapse onto both MGT and components of its downstream pre-motor circuits. Optogenetic activation of UMGT1 suppresses thoracic cleaning, representing a mechanism by which mechanosensory stimuli on other body parts could take precedence in the grooming hierarchy. We also mapped the pre-motor circuit downstream of MGT, including inhibitory feedback connections that may enable rhythmicity and coordination of limb movement during thoracic grooming.

neuroscience↗

Behavioral evidence for nested central pattern generator control of Drosophila grooming

Central pattern generators (CPGs) are neurons or neural circuits that produce periodic output without requiring patterned input. More complex behaviors can be assembled from simpler subroutines, and nested CPGs have been proposed to coordinate their repetitive elements, organizing control over different time-scales. Here, we use behavioral experiments to establish that Drosophila grooming may be controlled by nested CPGs. On a short time-scale (5-7 Hz), flies execute periodic leg sweeps and rubs. More surprisingly, transitions between bouts of head cleaning and leg rubbing are also periodic on a longer time-scale (0.3 - 0.6 Hz). We examine grooming at a range of temperatures to show that the frequencies of both oscillations increase - a hallmark of CPG control - and also that the two time-scales increase at the same rate, indicating that the nested CPGs may be linked. This relationship also holds when sensory drive is held constant using optogenetic activation, but the rhythms can decouple in spontaneously grooming flies, showing that alternative control modes are possible. Loss of sensory feedback does not disrupt periodicity but slows the longer time-scale alternation. Nested CPGs simplify generation of complex but repetitive behaviors, and identifying them in Drosophila grooming presents an opportunity to map the neural circuits that constitute them.

neuroscience↗

Variation and variability in Drosophila grooming behavior

Behavioral differences can be observed between species or populations (variation) or between individuals in a genetically similar population (variability). Here, we investigate genetic differences as a possible source of variation and variability in Drosophila grooming. Grooming confers survival and social benefits. Grooming features of five Drosophila species exposed to a dust irritant were analyzed. Aspects of grooming behavior, such as anterior to posterior progression, were conserved between and within species. However, significant differences in activity levels, proportion of time spent in different cleaning movements, and grooming syntax were identified between species. All species tested showed individual variability in the order and duration of action sequences. Genetic diversity was not found to correlate with grooming variability within a species: melanogaster flies bred to increase or decrease genetic heterogeneity exhibited similar variability in grooming syntax. Individual flies observed on consecutive days also showed grooming sequence variability. Standardization of sensory input using optogenetics reduced but did not eliminate this variability. In aggregate, these data suggest that sequence variability may be a conserved feature of grooming behavior itself. These results also demonstrate that large genetic differences result in distinguishable grooming phenotypes (variation), but that genetic heterogeneity within a population does not necessarily correspond to an increase in the range of grooming behavior (variability).

animal behavior and cognition↗

Simultaneous Activation Of Parallel Sensory Pathways Promotes A Grooming Sequence In Drosophila

A central model that describes how behavioral sequences are produced features a neural architecture that readies different movements simultaneously, and a mechanism where prioritized suppression between the movements determines their sequential performance. We previously described a model whereby suppression drives a Drosophila grooming sequence that is induced by simultaneous activation of different sensory pathways that each elicit a distinct movement (Seeds et al. 2014). Here, we confirm this model using transgenic expression to identify and optogenetically activate sensory neurons that elicit specific grooming movements. Simultaneous activation of different sensory pathways elicits a grooming sequence that resembles the naturally induced sequence. Moreover, the sequence proceeds after the sensory excitation is terminated, indicating that a persistent trace of this excitation induces the next grooming movement once the previous one is performed. This reveals a mechanism whereby parallel sensory inputs can be integrated and stored to elicit a delayed and sequential grooming response.

neuroscience↗