Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies

Ishikawa, Yuki; Okamoto, Natsuki; Nakamura, Masamichi; Kim, Hyunsoo; Kamikouchi, Azusa

doi:10.3389/fncir.2017.00046

Cited by 29 publications

(33 citation statements)

References 56 publications

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“…Johnston’s organ neurons are cholinergic (Ishikawa et al, 2017; Yasuyama and Salvaterra, 1999), so we first tested the effect of pharmacologically blocking nicotinic acetylcholine receptors. This had only a small effect on A2 cell responses (peak responses to step displacements were reduced by 21% on average, n=5 cells, p=0.06, two-sided sign-rank test, data not shown).…”

Section: Resultsmentioning

confidence: 99%

“…Flies rely on this organ to evaluate courtship song (Ishikawa et al, 2017; Kamikouchi et al, 2009; Yorozu et al, 2009), to analyze wind cues (Bhandawat et al, 2010; Budick et al, 2007; Duistermars and Frye, 2008; Yorozu et al, 2009), to detect touch (Hampel et al, 2015), and to monitor their own dynamic motor performance and posture (Kamikouchi et al, 2009; Mamiya and Dickinson, 2015; Mamiya et al, 2011). Johnston’s organ is thus conceptually analogous to the vertebrate auditory, somatosensory, proprioceptive, and vestibular sense organs.…”

Section: Introductionmentioning

confidence: 99%

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Active Mechanisms of Vibration Encoding and Frequency Filtering in Central Mechanosensory Neurons

Azevedo

Wilson

2017

Neuron

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Summary To better understand biophysical mechanisms of mechanosensory processing, we investigated two cell types in the Drosophila brain (A2 and B1 cells) that are postsynaptic to antennal vibration receptors. A2 cells receive excitatory synaptic currents in response to both directions of movement – thus twice per vibration cycle. The membrane acts as a lowpass-filter, so that voltage and spiking mainly track the vibration envelope rather than individual cycles. By contrast, B1 cells are excited by only forward or backward movement, meaning they are sensitive to vibration phase. They receive oscillatory synaptic currents at the stimulus frequency, and they bandpass-filter these inputs to favor specific frequencies. Different cells prefer different frequencies, due to differences in their voltage-gated conductances. Both Na+ and K+ conductances suppress low-frequency synaptic inputs, so cells with larger voltage-gated conductances prefer higher frequencies. These results illustrate how membrane properties and voltage-gated conductances can extract distinct stimulus features into parallel channels.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Active Mechanisms of Vibration Encoding and Frequency Filtering in Central Mechanosensory Neurons

Azevedo

Wilson

2017

Neuron

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“…In order to assess the generation of JO neurons in adult Drosophila, we used P-MARCM containing iav-GAL4 line (Kwon et al, 2010) (Ishikawa et al, 2017). iav (inactive) is a transient receptor potential (TRP) vanilloid channel expressed exclusively in the cilia of chordotonal neurons, and is essential for mechano-transduction in hearing (Gong et al, 2004).…”

Section: Identification Of Jo Neurogenesis By P-marcmmentioning

confidence: 99%

“…JO develops under conserved genetic programs with and act as counterparts to mammalian hair-cells and their innervating neurons, by supporting auditory and vestibular functions (Boekhoff-Falk, 2005;Eberl and Boekhoff-Falk, 2007;Kamikouchi et al, 2009;Li et al, 2018;Sun et al, 2009;Wang et al, 2002). Drosophila represents a compelling platform to accelerate research on functional regeneration of mechanosensory cells due to genome-wide available due to unparalleled available genetic tools, a detailed characterization of JO neurons at the circuitry-and behavioral-level (Ishikawa et al, 2017;Kamikouchi et al, 2006;Lai et al, 2012;Matsuo et al, 2016;Vaughan et al, 2014) and simple scalability at low cost. Yet, turnover of JO neurons has not been reported thus far.…”

Section: Introductionmentioning

confidence: 99%

Mechanosensory neuron regeneration in adult Drosophila

Fernández-Hernández

Marsh

Bonaguidi

2019

Preprint

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Auditory and vestibular mechanosensory hair cells in the adult mammalian inner ear do not regenerate following injury or ageing, inducing irreversible hearing loss and balance disorders for millions of people. Research on model systems showing replacement of mechanosensory cells can provide mechanistic insight to develop new regenerative therapies. Here we developed new lineage tracing systems to reveal the generation of mechanosensory neurons (Johnston's Organ, JO) in the antennae of intact adult Drosophila. New JO neurons develop cilia, express an essential mechano-transducer gene and target central brain circuitry. Furthermore, we identified low-level JO self-replication as a new mechanism of neuronal plasticity. Overall, our findings introduce a new platform to expedite the research of mechanisms and compounds mediating mechanosensory cell regeneration.

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“…Yet it remains unclear how sensory topography interfaces with neural circuits to influence behavior (Kaas, 1997;Thivierge and Marcus, 2007). mechanical forces that move the antennae, including sound, wind, gravity, wing beats, and tactile stimuli (Hampel et al, 2015;Ishikawa et al, 2017;Kamikouchi et al, 2009;Mamiya and Dickinson, 2015;Matsuo et al, 2014;Patella and Wilson, 2018;Yorozu et al, 2009). The ability of the JO to respond to these different stimuli is conferred by about 480 mechanosensory neurons called JONs (Kamikouchi et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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

Hampel

Eichler

Yamada

et al. 2020

Preprint

Self Cite

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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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Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies

Cited by 29 publications

References 56 publications

Active Mechanisms of Vibration Encoding and Frequency Filtering in Central Mechanosensory Neurons

Active Mechanisms of Vibration Encoding and Frequency Filtering in Central Mechanosensory Neurons

Mechanosensory neuron regeneration in adult Drosophila

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

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