Encoding of wind direction by central neurons in<i>Drosophila</i>

Suver, Marie P.; Matheson, Andrew M. M.; Sarkar, Sinekdha; Damiata, Matthew; Schoppik, David; Nagel, Katherine I.

doi:10.1101/504753

Cited by 12 publications

(27 citation statements)

References 60 publications

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“…Wind perception is crucial for navigation, including anemotaxis (following odors upwind) or flight in general. The LH receives projections from the wedge, a third-order mechanosensory region [ 8 , 14 , 74 , 75 , 76 ] ( Figure S6 A). Genetic activation of WEDPN1 (R37E08-GAL4) generates increased wing-flick motion and differential wing-angling [ 77 ] ( Figure S6 C).…”

Section: Discussionmentioning

confidence: 99%

“…All belonged to GABAergic lineages [ 25 ]. A further ∼10 neurons from the wedge brushed past the LH, including previously studied wind-sensitive WEDPNs [ 76 ]. We found that all types except type 7 had an axon in the LH and dendrites in the wedge, with spill-over into other ill-defined third-order mechanosensory neuropils in the inferior region of the ventrolateral protocerebrum ( Figure 6 D).…”

Section: Methodsmentioning

confidence: 99%

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Complete Connectomic Reconstruction of Olfactory Projection Neurons in the Fly Brain

et al. 2020

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Summary Nervous systems contain sensory neurons, local neurons, projection neurons, and motor neurons. To understand how these building blocks form whole circuits, we must distil these broad classes into neuronal cell types and describe their network connectivity. Using an electron micrograph dataset for an entire Drosophila melanogaster brain, we reconstruct the first complete inventory of olfactory projections connecting the antennal lobe, the insect analog of the mammalian olfactory bulb, to higher-order brain regions in an adult animal brain. We then connect this inventory to extant data in the literature, providing synaptic-resolution “holotypes” both for heavily investigated and previously unknown cell types. Projection neurons are approximately twice as numerous as reported by light level studies; cell types are stereotyped, but not identical, in cell and synapse numbers between brain hemispheres. The lateral horn, the insect analog of the mammalian cortical amygdala, is the main target for this olfactory information and has been shown to guide innate behavior. Here, we find new connectivity motifs, including axo-axonic connectivity between projection neurons, feedback, and lateral inhibition of these axons by a large population of neurons, and the convergence of different inputs, including non-olfactory inputs and memory-related feedback onto third-order olfactory neurons. These features are less prominent in the mushroom body calyx, the insect analog of the mammalian piriform cortex and a center for associative memory. Our work provides a complete neuroanatomical platform for future studies of the adult Drosophila olfactory system.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Complete Connectomic Reconstruction of Olfactory Projection Neurons in the Fly Brain

et al. 2020

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“…In Drosophila , the wedge receives direct input from antennal mechanosensory neurons and input from secondary neurons of the antennal mechanosensory and motor center (Ito et al, ). Patch‐clamp recordings showed that wedge neurons in Drosophila are sensitive to wind direction by integrating mechanosensory input from both antennae (Suver et al, ). Extracellular recordings in the cockroach Blaberus suggest that CX neurons receive prominent mechanosensory input from the antennae, but whether these responses, likewise, reflect spatial tactile information, remains to be seen (Ritzmann, Ridgel, & Pollak, ).…”

Section: Discussionmentioning

confidence: 99%

Neuroarchitecture of the central complex of the desert locust: Tangential neurons

Hadeln

Hensgen

Bockhorst

et al. 2019

J of Comparative Neurology

111

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The central complex (CX) comprises a group of midline neuropils in the insect brain, consisting of the protocerebral bridge (PB), the upper (CBU) and lower division (CBL) of the central body and a pair of globular noduli. It receives prominent input from the visual system and plays a major role in spatial orientation of the animals. Vertical slices and horizontal layers of the CX are formed by columnar, tangential, and pontine neurons.While pontine and columnar neurons have been analyzed in detail, especially in the fruit fly and desert locust, understanding of the organization of tangential cells is still rudimentary. As a basis for future functional studies, we have studied the morphologies of tangential neurons of the CX of the desert locust Schistocerca gregaria. Intracellular dye injections revealed 43 different types of tangential neuron, 8 of the PB, 5 of the CBL, 24 of the CBU, 2 of the noduli, and 4 innervating multiple substructures. Cell bodies of these neurons were located in 11 different clusters in the cell body rind. Judging from the presence of fine versus beaded terminals, the vast majority of these neurons provide input into the CX, especially from the lateral complex (LX), the superior protocerebrum, the posterior slope, and other surrounding brain areas, but not directly from the mushroom bodies. Connections are largely subunit-and partly layer-specific. No direct connections were found between the CBU and the CBL. Instead, both subdivisions are connected in parallel with the PB and distinct layers of the noduli.

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“…Our study advances our understanding of the breadth of behaviors that are influenced by the JONs. The JO-C/E neurons were previously implicated in such behaviors as wind-induced suppression of locomotion, wind-guided orientation, gravitaxis, flight, and antennal grooming ( Hampel et al, 2015 ; Kamikouchi et al, 2009 ; Mamiya and Dickinson, 2015 ; Suver et al, 2019 ; Yorozu et al, 2009 ). Our finding that optogenetic activation of the JO-C/E neurons results in wing flapping ( Figure 6B,C,D ) is intriguing, given that these neurons were previously shown to detect wing beats and then modulate wing movements during flight ( Mamiya and Dickinson, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

“…Subpopulations of JONs are selectively excited by different vibrational frequencies or by sustained displacements of the antennae and send their projections into discrete zones in the CNS ( Kamikouchi et al, 2006 ). In accordance with their diverse physiological tuning properties, the JONs are implicated in controlling diverse behaviors including courtship, locomotion, gravitaxis, wind-guided orientation, escape, flight, and grooming ( Hampel et al, 2015 ; Kamikouchi et al, 2009 ; Lehnert et al, 2013 ; Mamiya et al, 2011 ; Mamiya and Dickinson, 2015 ; Suver et al, 2019 ; Tootoonian et al, 2012 ; Vaughan et al, 2014 ; Yorozu et al, 2009 ). However, efforts to define how the different JONs interface with downstream neural circuitry to influence these behaviors have been hampered by the incomplete description of the morphologically heterogeneous JON types within each subpopulation ( Kamikouchi et al, 2006 ; Kim et al, 2020 ).…”

Section: Introductionmentioning

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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Encoding of wind direction by central neurons inDrosophila

Cited by 12 publications

References 60 publications

Complete Connectomic Reconstruction of Olfactory Projection Neurons in the Fly Brain

Complete Connectomic Reconstruction of Olfactory Projection Neurons in the Fly Brain

Neuroarchitecture of the central complex of the desert locust: Tangential neurons

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

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