Neuronal Constituents and Putative Interactions Within the Drosophila Ellipsoid Body Neuropil

Omoto, Jaison J.; Nguyen, Bao-Chau Minh; Kandimalla, Pratyush; Lovick, Jennifer K.; Donlea, Jeffrey M.; Hartenstein, Volker

doi:10.3389/fncir.2018.00103

Cited by 72 publications

(183 citation statements)

References 92 publications

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“…Both R2 and R4m ring neuron populations target the outer central domain of the EB, albeit following different trajectories (Fig. 6A,B) (Omoto et al, 2017(Omoto et al, , 2018. As with TuBu s micro-glomerular outputs, we found that only a subset of R2 neurons in the BUs were modulated by polarized light, with above-threshold PSI values typically in a medial cluster with a preferred angle of polarization (AoP) around 45° (Fig.…”

Section: R4m Ring Neurons Receive Polarization-tuned Responses From Tmentioning

confidence: 67%

“…6A), where their arborizations have a circular form and are both dendritic and axonal ( Fig. 6B) (Hanesch et al, 1989;Omoto et al, 2018). We recorded calcium activity in the dendrites of two populations of ring neurons in the bulb, one innervating the medial two-thirds of the BUs (R2; R19C08-Gal4) and one innervating the BUa (R4m; R34H10-Gal4) (Fig.…”

Section: R4m Ring Neurons Receive Polarization-tuned Responses From Tmentioning

confidence: 99%

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A visual pathway for skylight polarization processing inDrosophila

Hardcastle

Omoto

Kandimalla

et al. 2020

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SUMMARYMany insects use patterns of polarized light in the sky to orient and navigate. Here we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly’s sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the ‘sky compass’ pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

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Section: R4m Ring Neurons Receive Polarization-tuned Responses From Tmentioning

confidence: 67%

Section: R4m Ring Neurons Receive Polarization-tuned Responses From Tmentioning

confidence: 99%

A visual pathway for skylight polarization processing inDrosophila

Hardcastle

Omoto

Kandimalla

et al. 2020

Preprint

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“…In Drosophila, this tethering is thought to come from a large population of inhibitory ring neurons (Hanesch et al, 1989;Homberg et al, 2018;Lin et al, 2013;Omoto et al, 2018;Xie et al, 2017;Young and Armstrong, 2010). However, this has not yet been verified experimentally.…”

Section: Ring Neurons Tether the Compass To Visual Scenes By Selectivmentioning

confidence: 99%

“…A potential complication is that there are many types of ring neurons, only some of which are visually tuned (Homberg et al, 2011;Omoto et al, 2017;Omoto et al, 2018;Seelig and Jayaraman, 2013;Shiozaki and Kazama, 2017;Sun et al, 2017) To identify appropriate visual ring neurons to reconstruct in the EM dataset, we performed stochastic labeling of broad ring neuron lines using the FLP-out technique ( Figure S4A) (Golic and Lindquist, 1989) (see Methods). This technique allows for individual neurons to be tagged, and here we used it to express GCaMP6f in single neurons in order to monitor their Ca 2+ activity.…”

Section: Ring Neurons Tether the Compass To Visual Scenes By Selectivmentioning

confidence: 99%

The neuroanatomical ultrastructure and function of a biological ring attractor

Turner-Evans

Jensen

Ali

et al. 2019

Preprint

105

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Neural representations of head direction have been discovered in many different species. A large body of theoretical work has proposed that the dynamics associated with these representations might be generated, maintained, and updated by recurrent network structures called ring attractors. Ring attractor models rely on specific assumptions about the structure of excitatory and inhibitory connectivity. These assumptions have been difficult to test directly. We therefore performed electron-microscopy-based circuit reconstruction and RNA profiling of identified cell types in the heading direction system of Drosophila melanogaster to directly examine excitatory and inhibitory synaptic connectivity, generating a dataset that should serve as a reference for future functional studies of the network. Consistent with several theoretical models, we identified network motifs that have been hypothesized to maintain the heading representation in darkness, update it when the animal turns, and tether it to visual cues. Genetically targeted two-photon calcium imaging and thermogenetic perturbation of the constituent neuron types during behavior provided additional support for these functional roles. However, we also discovered network motifs absent in current models, including a surprising degree of recurrence between arbors of different neurons with mixed pre-and post-synaptic specializations. Overall, our results confirm that the Drosophila heading direction network contains the core components of a ring attractor while also revealing unpredicted structural features that might enable the heading system to accurately track the animal's heading with a small number of neurons. Importantly, however, these and other models of attractor networks in the fly have assumed the circuit's connectivity based on relatively indirect evidence (Cope et al., 2017;Han et al., 2019;Kakaria and de Bivort, 2017;Kim et al., 2017;Su et al., 2017;Turner-Evans et al., 2017). For example, the location of pre-and post-synaptic arbors has been inferred from whether neural processes visible in light-microscopic images seem spine-or bouton-like in specific substructures (Hanesch et al., 1989;Lin et al., 2013;Wolff et al., 2015). The hypothesized connectivity of the circuit has then been derived from light-level overlap between the putatively pre-and post-synaptic arbors of neurons . In Drosophila, such conclusions have been bolstered by employing GFP-reconstitution-acrosssynaptic-partners (GRASP) (Xie et al., 2017) and trans-Tango (Omoto et al., 2018) techniques. Although both GRASP and trans-Tango are powerful techniques, their reliability and accuracy when used to estimate pairwise connectivity is limited (Lee et al., 2017; Talay et al., 2017). Similarly, measurements of functional connectivity by optogenetic stimulation of one neuron type and calcium imaging of another (Franconville et al., 2018) cannot conclusively establish the presence or absence of monosynaptic connectivity.In the current study, we established the synaptic-and cellular-resolution str...

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“…We expressed this construct in Ring (R) neurons, GABAergic neurons that send sensory input to the central complex 20 . R neurons are divided into types based on morphology 21 , here we focused on the R2 type. We expressed SPARC2-D-CsChrimson::tdTomato in a subset of R2 neurons (Figures 2F-H”).…”

Section: Main Textmentioning

confidence: 99%

SPARC: a method to genetically manipulate precise proportions of cells

Isaacman-Beck

Cfr

et al. 2019

Preprint

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17Many experimental approaches rely on controlling gene expression in select subsets of 18 cells within an individual animal. However, reproducibly targeting transgene expression 19 to specific fractions of a genetically-defined cell-type is challenging. We developed 20Sparse Predictive Activity through Recombinase Competition (SPARC), a generalizable 21 toolkit that can express any effector in precise proportions of post-mitotic cells in 22Drosophila. Using this approach, we demonstrate targeted expression of many 23 S2) 7 . The core of this toolkit is a set of bistable UAS-driven constructs that can be 46 switched on or off in different relative proportions of cells, depending on their 47 expression of each SPARC construct in one of the largest genetically-defined 62 populations of neurons in the Drosophila optic lobe, T4 and T5 cells 11 , in animals that 63 express PhiC31 pan-neuronally. Across SPARC-GCaMP6f variants, we observed 64 progressively fewer labeled neurons (Fig. 1C-E). SPARC-attP60-GCaMP6f labeled 65 many overlapping neurons, SPARC-attP38-GCaMP6f labeled an intermediate number 66of neurons and SPARC-attP34-GCaMP6f labeled individual neurons whose dendrites 67 could be visualized (Fig 1E inset). We therefore named these variants SPARC-D individual T5 cells relied on laborious FlpOut approaches that required titrated and 108 temporally precise heat shocks of Drosophila larvae to restrict effector expression to a 109 subset of cells [16][17][18] . In contrast, the SPARC method consistently labeled fewer T5 110 neurons, and labeled them more sparsely, than the sparsest FlpOut labeling using brief 111 and developmentally late heat-shock ( Fig. 1E, 2A,B). More importantly, when we 112 imaged visually-evoked Ca 2+ responses in regions of interest (ROIs) representing T5 113 dendrites, we observed that the fluorescent signals from SPARC-labeled ROIs were depolarized ( Figure 2I, J). Indeed, tdTomato -R2 neurons were slightly hyperpolarized 130 by light ( Figure 2I, J), implying that these R2 neurons were postsynaptic to other R2 131 neurons that express CsChrimson. Thus, the SPARC system enables optogenetic 132 activation of sparse cell populations within a single cell type, allowing us to discover 133 evidence for mutual inhibitory interactions within a cell type. Although it was already 134 known that some R neuron types inhibit other R types 20 , it was not previously known 135 that there is mutual inhibition between R neurons of the same type.

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Neuronal Constituents and Putative Interactions Within the Drosophila Ellipsoid Body Neuropil

Cited by 72 publications

References 92 publications

A visual pathway for skylight polarization processing inDrosophila

A visual pathway for skylight polarization processing inDrosophila

The neuroanatomical ultrastructure and function of a biological ring attractor

SPARC: a method to genetically manipulate precise proportions of cells

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