Spatial Comparisons of Mechanosensory Information Govern the Grooming Sequence in Drosophila

Zhang, Neil; Guo, Li; Simpson, Jeffrey H.

doi:10.1016/j.cub.2020.01.045

Cited by 31 publications

(56 citation statements)

References 53 publications

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“…dust) and mechanical displacements of the antennae ( Hampel et al, 2015 ; Phillis et al, 1993 ; Seeds et al, 2014 ). Moreover, neuronal silencing experiments have linked the JO-C/E neurons to the grooming response to dust and the JO-F neurons to the grooming response to antennal displacement: Zhang et al, 2020 recently reported that dust-elicited grooming could be disrupted by expression of tetanus toxin using a driver line that appears to target the JO-C/E neurons, while we previously found that expression of tetanus toxin in JO-F neurons (using aJO-spGAL4-1) disrupted the grooming response to displacements of the antennae ( Hampel et al, 2015 ). These studies suggest that the JON subpopulations detect these different mechanical stimuli and initiate the grooming response.…”

Section: Discussionmentioning

confidence: 99%

Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae

Hampel

Eichler

Yamada

et al. 2020

eLife

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Diverse mechanosensory neurons detect different mechanical forces that can impact animal behavior. Yet our understanding of the anatomical and physiological diversity of these neurons and the behaviors that they influence is limited. We previously discovered that grooming of the Drosophila melanogaster antennae is elicited by an antennal mechanosensory chordotonal organ, the Johnston's organ (JO) (Hampel et al., 2015). Here, we describe anatomically and physiologically distinct JO mechanosensory neuron subpopulations that each elicit antennal grooming. We show that the subpopulations project to different, discrete zones in the brain and differ in their responses to mechanical stimulation of the antennae. Although activation of each subpopulation elicits antennal grooming, distinct subpopulations also elicit the additional behaviors of wing flapping or backward locomotion. Our results provide a comprehensive description of the diversity of mechanosensory neurons in the JO, and reveal that distinct JO subpopulations can elicit both common and distinct behavioral responses.

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Section: Discussionmentioning

confidence: 99%

Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae

Hampel

Eichler

Yamada

et al. 2020

eLife

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“…Interestingly, the JO-CE neurons are implicated in the grooming response to dust, while the JO-F neurons are implicated in the response to antennal displacements. A recent study showed that expression of tetanus toxin (TNT) using a driver line that appears to target JO-CE neurons disrupted dust induced grooming (Zhang et al, 2020). We found that expression of TNT using a driver that mostly targets the JO-F neurons (aJO-spGAL4-1) disrupted the grooming response to displacements of the antennae (Hampel et al, 2015).…”

Section: Diverse Jon Subpopulations Converge Onto the Antennal Commanmentioning

confidence: 79%

Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits grooming

Hampel

Eichler

Yamada

et al. 2020

Preprint

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Diverse subpopulations of mechanosensory neurons detect different mechanical forces and influence behavior. How these subpopulations connect with central circuits to influence behavior remains an important area of study. We previously discovered a neural circuit that elicits grooming of the Drosophila melanogaster antennae that is activated by an antennal mechanosensory chordotonal organ, the Johnston's organ (JO) (Hampel et al., 2015). Here, we describe anatomically and physiologically distinct JO mechanosensory neuron subpopulations and define how they interface with the circuit that elicits antennal grooming. We show that the subpopulations project to distinct zones in the brain and differ in their responses to mechanical stimulation of the antennae. Each subpopulation elicits grooming through direct synaptic connections with a single interneuron in the circuit, the dendrites of which span the different mechanosensory afferent projection zones. Thus, distinct JO subpopulations converge onto the same neural circuit to elicit a common behavioral response.The fruit fly (Drosophila melanogaster) Johnston's organ (JO) is a chordotonal organ in the antennae that can be studied to address this outstanding question. The JO detects diverse types of subpopulations are each known to consist of morphologically heterogeneous JON types that have not been completely described (Kamikouchi et al., 2006), we first define their morphological diversity by reconstructing major portions of each subpopulation from an EM volume of the fly brain (Zheng et al., 2018). We next produce transgenic driver lines that selectively target expression in each subpopulation. These lines enable us to visualize the distribution of the different subpopulations in the antennae and determine that they respond differently to mechanical stimuli. Optogenetic activation experiments confirm our previous finding that each JON subpopulation can elicit grooming of the antennae (Hampel et al., 2015). However, we report here that one of the subpopulations also elicits an avoidance response, whereas the other elicits wing flapping movements. Finally, by employing EM reconstructions and functional imaging experiments, we determine that JONs within each subpopulation are synaptically and functionally connected with the antennal command circuit through the same interneuron (aBN1). These results provide a comprehensive description of the topography of the JO, and reveal how different JON subpopulations whose projections occupy different points in topographical space can converge on the same neural circuit to elicit a similar behavioral response. Results and discussion Electron microscopy-based reconstruction of different JON subpopulationsWe first sought to define the morphological diversity of the neurons within each JON subpopulation as a prerequisite for understanding how the subpopulations interface with the antennal command circuit. JONs project from the antennae through the antennal nerve into a region of the SEZ called the antennal mechanosensory and motor ce...

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“…We previously demonstrated that this manipulation induces grooming, beginning with the anterior body parts, and alternating between bouts of head cleaning and front leg rubbing (Hampel, McKellar, Simpson, & Seeds, 2017; Zhang, Guo, & Simpson, 2020). Here, we combine optogenetic activation for constant sensory input with temperature control to show that both individual leg movements and bout-level alternations increase in a correlated manner.…”

Section: Resultsmentioning

confidence: 99%

Behavioral evidence for nested central pattern generator control ofDrosophilagrooming

Ravbar

Zhang

Simpson

2020

Preprint

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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, simplifying control over different time-scales. Here, we use behavioral experiments to establish that Drosophila grooming may be controlled by nested CPGs. On the 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 decouple in spontaneously grooming flies, showing that alternative control modes are possible. 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.

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Spatial Comparisons of Mechanosensory Information Govern the Grooming Sequence in Drosophila

Cited by 31 publications

References 53 publications

Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae

Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae

Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits grooming

Behavioral evidence for nested central pattern generator control ofDrosophilagrooming

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