Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs

Wu, Ming‐Chi; Nern, Aljoscha; Williamson, W. Ryan; Morimoto, Mitsuru; Reiser, Michael B.; Card, Gwyneth M; Rubin, Gerald M.

doi:10.7554/elife.21022

Cited by 257 publications

(575 citation statements)

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“…The lobula contains more than 22 types of visual projection neurons (VPNs) including lobula columnar (LC) neurons that project to the ventrolateral protocerebrum (VLPR) and form synapse-rich output domains called optic glomeruli for their structural similarity to olfactory glomeruli [4,15,16]. Neurons downstream of LCs that interconnect multiple optic glomeruli in the central brain respond to small objects [17], raising the possibility that select LCs may themselves be tuned to small objects.…”

Section: Resultsmentioning

confidence: 99%

Object-Detecting Neurons in Drosophila

2017

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SUMMARY Many animals rely on vision to detect objects such as conspecifics, predators, and prey. Hypercomplex cells found in feline cortex and small target motion detectors found in dragonfly and hoverfly optic lobes demonstrate robust tuning for small objects with weak or no response to larger objects or movement of the visual panorama [1–3]. However, the relationship between anatomical, molecular, and functional properties of object detection circuitry is not understood. Here, we characterize a specialized object detector in Drosophila, the lobula columnar neuron LC11 [4]. By imaging calcium dynamics with two-photon excitation microscopy we show that LC11 responds to the omni-directional movement of a small object darker than the background, with little or no responses to static flicker, vertically elongated bars, or panoramic gratings. LC11 dendrites innervate multiple layers of the lobula, and each dendrite spans enough columns to sample 75-degrees of visual space, yet the area that evokes calcium responses is only 20-degrees wide, and shows robust responses to a 2.2-degree object spanning less than half of one facet of the compound eye. The dendrites of neighboring LC11s encode object motion retinotopically, but the axon terminals fuse into a glomerular structure in the central brain where retinotopy is lost. Blocking inhibitory ionic currents abolishes small object sensitivity and facilitates responses to elongated bars and gratings. Our results reveal high acuity object motion detection in the Drosophila optic lobe.

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Section: Resultsmentioning

confidence: 99%

Object-Detecting Neurons in Drosophila

2017

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“…We posit that the object-tracking tracking system should 1) exhibit no directional selectivity (Figure S1A), 2) have narrow bilateral receptive fields offset by approximately ±45° (Figure 2A), 3) be sensitive to bar motion irrespective of wide-field motion (Figure 5), and 4) integrate position error (Figure 2E). Small-object sensitive neurons have recently been discovered in the lobula of Drosophila therefore the lobula may be a good candidate to implement tuning of visually-guided saccades during object fixation [45, 46]. In contrast, the wide-field system should respond weakly to bar motion (Figure 4A) and integrate wide-field motion velocity.…”

Section: Discussionmentioning

confidence: 99%

Drosophila Spatiotemporally Integrates Visual Signals to Control Saccades

2017

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SUMMARY Like many visually active animals including humans, flies generate both smooth and rapid, saccadic movements to stabilize their visual gaze. How rapid body saccades and smooth movement interact for simultaneous object pursuit and gaze stabilization is not understood. We directly observed these interactions in magnetically-tethered Drosophila free to rotate about the yaw axis. A moving bar elicited sustained bouts of saccades following the bar, with surprisingly little smooth movement. By contrast, a moving panorama elicited robust smooth movement interspersed with occasional optomotor saccades. The amplitude, angular velocity, and torque transients of bar-fixation saccades were finely tuned to the speed of bar motion, and were triggered by a threshold in the temporal integral of the bar error angle, rather than its absolute retinal position error. Optomotor saccades were tuned to the dynamics of panoramic image motion, and were triggered by a threshold in the integral of velocity over time. A hybrid control model based on integrated motion cues simulates saccade trigger and dynamics. We propose a novel algorithm for tuning fixation saccades in flies.

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“…Visual projection neurons (VPNs) convey information from lower to higher-order visual processing centers, called optic glomeruli, which are located more centrally (Otsuna and Ito, 2006). Relatively little is known about computations in the optic glomeruli, but recent studies suggest a role in second-order motion processing (Zhang et al, 2013) and processing that mediates natural avoidance behaviors (Wu et al, 2016). Specific optic glomeruli, such as the ventrolateral protocereberum (Ito et al, 2014), send projections back to the lobula and medulla, as well as reciprocated projections to other central structures (Otsuna and Ito, 2006; Shih et al, 2015).…”

Section: Methodsmentioning

confidence: 99%

Isoflurane Impairs Low-Frequency Feedback but Leaves High-Frequency Feedforward Connectivity Intact in the Fly Brain

Cohen

Swinderen

Tsuchiya

2018

eNeuro

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Hierarchically organized brains communicate through feedforward (FF) and feedback (FB) pathways. In mammals, FF and FB are mediated by higher and lower frequencies during wakefulness. FB is preferentially impaired by general anesthetics in multiple mammalian species. This suggests FB serves critical functions in waking brains. The brain of Drosophila melanogaster (fruit fly) is also hierarchically organized, but the presence of FB in these brains is not established. Here, we studied FB in the fly brain, by simultaneously recording local field potentials (LFPs) from low-order peripheral structures and higher-order central structures. We analyzed the data using Granger causality (GC), the first application of this analysis technique to recordings from the insect brain. Our analysis revealed that low frequencies (0.1–5 Hz) mediated FB from the center to the periphery, while higher frequencies (10–45 Hz) mediated FF in the opposite direction. Further, isoflurane anesthesia preferentially reduced FB. Our results imply that the spectral characteristics of FF and FB may be a signature of hierarchically organized brains that is conserved from insects to mammals. We speculate that general anesthetics may induce unresponsiveness across species by targeting the mechanisms that support FB.

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Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs

Cited by 257 publications

References 100 publications

Object-Detecting Neurons in Drosophila

Object-Detecting Neurons in Drosophila

Drosophila Spatiotemporally Integrates Visual Signals to Control Saccades

Isoflurane Impairs Low-Frequency Feedback but Leaves High-Frequency Feedforward Connectivity Intact in the Fly Brain

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