Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae
- University of Puerto Rico Medical Sciences Campus, Puerto Rico
- Nagoya University, Japan
- University of Vermont, United States
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.
Data availability
Neuron reconstructions will be made available on https://v2.virtualflybrain.org/
Article and author information
Author details
Funding
Whitehall Foundation (2017-12-69)
- Andrew M Seeds
National Institute on Minority Health and Health Disparities (MD007600)
- Andrew M Seeds
National Institute of General Medical Sciences (GM103642)
- Stefanie Hampel
- Andrew M Seeds
Puerto Rico Science, Technology and Research Trust (2020-00195)
- Andrew M Seeds
National Science Foundation (HRD-1736019)
- Andrew M Seeds
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Ronald L Calabrese, Emory University, United States
Version history
- Received: June 15, 2020
- Accepted: October 25, 2020
- Accepted Manuscript published: October 26, 2020 (version 1)
- Version of Record published: November 9, 2020 (version 2)
Copyright
© 2020, Hampel et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae
eLife 9:e59976.
https://doi.org/10.7554/eLife.59976
Further reading
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- Neuroscience
Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.
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- Neuroscience
Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.
