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Cited by 35Neurobiology and Insect Physiology ResearchIon Channels and ReceptorsNeuroscience and Neuropharmacology Research

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

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Hampel, Stefanie, Eichler, Katharina, Yamada, Daichi, Bock, Davi D, Kamikouchi, Azusa, Seeds, Andrew M·2020·eLife
DOI 10.7554/elife.59976PMC PMC7652415
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Abstract

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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  • Computational activation of mechanosensory neurons predicts activation of a small set of neurons comprising the antennal grooming circuit, and accurately describes the circuit response upon activation of different mechanosensory subtypes.

    “Additionally, we applied this model to mechanosensory circuits and found that computational activation of mechanosensory neurons predicts activation of a small set of neurons comprising the antennal grooming circuit, and accurately describes the circuit response upon activation of different mechanosensory subtypes6–10.”

    From A Drosophila computational brain model reveals sensorimotor processing (2024) · cites this paper as [7]

    The Discussion (‘Neural circuit basis of JON-induced antennal grooming’; page not provided) describes an antennal-grooming circuit comprising three interneuron types. The Results (‘Activation of JO-C/E or JO-F neurons’; page not provided) show that activating different mechanosensory subtypes elicits grooming. The paper does not test a computational model or establish the claimed accuracy of its predictions; the citing sentence presents those as the citing authors’ own findings. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • aBN1, aBN2, aDN1 and aDN2 were each identified and annotated from their previously described morphology.

    “aBN1, aBN2, aDN1 and aDN2 were each identified and annotated from their previously described morphology2,6,7.”

    From A Drosophila computational brain model reveals sensorimotor processing (2024) · cites this paper as [7]

    The Discussion section, “Neural circuit basis of JON-induced antennal grooming” (page unavailable), describes aBN1 and aBN2 as previously identified, morphologically distinct interneuron types. It describes aDNs only as a cluster of descending neurons; it does not identify aDN1 and aDN2 individually or say that all four neurons were annotated from their previously described morphology. The Methods’ morphology-based annotations concern JONs, not these four neurons. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • A total of 147 JONs belonging to classes JO-C, JO-E, JO-F and JO-mz were identified previously and described in the electron microscopy volume.

    “A total of 147 JONs belonging to classes JO-C, JO-E, JO-F and JO-mz were identified previously and described in the electron microscopy volume7.”

    From A Drosophila computational brain model reveals sensorimotor processing (2024) · cites this paper as [7]

    The Results and Materials and methods describe 147 JONs reconstructed in the EM volume, including seven JO-mz neurons. But they also identify JO-D neurons among the reconstructed population, which the citing sentence omits from its list of classes. (LLM, conf=0.89)

    Experimental — accuracy not yet measured

  • The antennal grooming circuit has well-defined sensory inputs and a discrete, easily quantified behavioural output: antennal grooming behaviour.

    “As with the feeding initiation circuit, the antennal grooming circuit has well-defined sensory inputs, and a discrete, easily quantified behavioural output: antennal grooming behaviour.”

    From A Drosophila computational brain model reveals sensorimotor processing (2024) · cites this paper as [7]

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Cited by

Sorted by citations

Authors
Hampel, S., Eichler, K., Yamada, D., Bock, D. D., Kamikouchi, A., & Seeds, A. M.
Affiliations
  • University of Puerto Rico, Medical Sciences Campus (PR)
  • Nagoya University (JP)
  • University of Vermont (US)
Corresponding author
  • Hampel, Stefanie
  • Seeds, Andrew M
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2020-10-26
Volume
9
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.59976
PMC
PMC7652415
OpenAlex
W3094308512
Cited by
35
References
12
Citations by year
2026: 2 · 2025: 6 · 2024: 8 · 2023: 14 · 2022: 3 · 2021: 2
FWCI
2.18
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • Apollo (cc-by)
Funders
  • Whitehall Foundation (2017-12-69)
  • National Institute on Minority Health and Health Disparities (MD007600)
  • National Institute of General Medical Sciences (GM103642)
  • Puerto Rico Science, Technology and Research Trust (2020-00195)
  • National Science Foundation (HRD-1736019)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
Johnston's organ, chordotonal organ, mechanosensory neurons, Drosophila melanogaster, neuronal subpopulations, neuronal heterogeneity, flapping wings, backward locomotion, mechanosensing, insect behavior
MeSH terms
Animals, Drosophila melanogaster, Female, Grooming, Male, Mechanoreceptors, Neurons, Sense Organs, Arthropod Antennae

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