Inhibitory Interactions and Columnar Inputs to an Object Motion Detector in Drosophila

Keleş, Mehmet F.; Hardcastle, Ben J.; Städele, Carola; Xiao, Qi; Frye, Mark A.

doi:10.1016/j.celrep.2020.01.061

Cited by 42 publications

(72 citation statements)

References 48 publications

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“…We utilised the grey strip paradigm to remove changes in target contrast, thus isolating long-range effects to those due to optic-flow and competition with other background features. In other insects, background motion may completely suppress neuronal responses, as observed in descending neurons (Nicholas et al 2018) and some lobula motion detectors (Keles et al 2020). Here we show that dragonfly STMD responses exhibit trial-by-trial variability, which our modelling suggests is due to selective attention rather than surround suppression.…”

Section: Discussionmentioning

confidence: 99%

Dragonfly visual neurons selectively attend to features in naturalistic scenes

Evans

Fabian

O’Carroll

et al. 2020

Preprint

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Aerial predators, such as the dragonfly, determine the position and movement of their prey even when embedded in natural scenes. This task is likely supported by a group of optic lobe neurons with responses selective for moving targets of less than a few degrees. These Small Target Motion Detector (STMD) neurons are tuned to target velocity and show profound facilitation in responses to targets that move along continuous trajectories. When presented with a pair of targets, some STMDs competitively select one of the alternatives as if the other does not exist.Here we describe intracellular responses of STMD neurons to the visual presentation of many potential alternatives within cluttered environments comprised of natural scenes. We vary both target contrast and the background scene, across a range of target and background velocities. We find that background motion affects STMD responses indirectly, via the competitive selection of background features. We find that robust target discrimination is limited to scenarios when the target velocity is matched to, or greater than, background velocity. Furthermore, STMD target discriminability is modified by background direction. Backgrounds that move in the neuron’s anti-preferred direction result in the least performance degradation.Significance StatementBiological brains solve the difficult problem of visually detecting and tracking moving features in cluttered environments. We investigated this neuronal processing by recording intracellularly from dragonfly visual neurons that encode the motion of small moving targets subtending less than a few degrees (e.g. prey and conspecifics). However, dragonflies live in a complex visual environment where background features may interfere with tracking by reducing target contrast or providing competitive cues. We find that selective attention towards features drives much of the neuronal response, with background clutter competing with target stimuli for selection. Moreover, the velocity of features is an important component in determining the winner in these competitive interactions.

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Section: Discussionmentioning

confidence: 99%

Dragonfly visual neurons selectively attend to features in naturalistic scenes

Evans

Fabian

O’Carroll

et al. 2020

Preprint

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“…If so, serotonin might change the spatial structure of surround inhibition as well as tip the balance between ON and OFF response components to favor ON stimulation. Cell-specific manipulation of Rdl and/or 5-HT2B might be used to test this hypothesis [109,132].…”

Section: Plos Geneticsmentioning

confidence: 99%

“…Calcium imaging was performed as previously described [132,143,144]. Briefly, flies were anesthetized at 4˚C and placed into a chemically etched metal shim within a larger custom-built fly holder.…”

Section: Live Cell Imagingmentioning

confidence: 99%

Serotonergic modulation of visual neurons in Drosophila melanogaster

et al. 2020

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Sensory systems rely on neuromodulators, such as serotonin, to provide flexibility for information processing as stimuli vary, such as light intensity throughout the day. Serotonergic neurons broadly innervate the optic ganglia of Drosophila melanogaster, a widely used model for studying vision. It remains unclear whether serotonin modulates the physiology of interneurons in the optic ganglia. To address this question, we first mapped the expression patterns of serotonin receptors in the visual system, focusing on a subset of cells with processes in the first optic ganglion, the lamina. Serotonin receptor expression was found in several types of columnar cells in the lamina including 5-HT2B in lamina monopolar cell L2, required for spatiotemporal luminance contrast, and both 5-HT1A and 5-HT1B in T1 cells, whose function is unknown. Subcellular mapping with GFP-tagged 5-HT2B and 5-HT1A constructs indicated that these receptors localize to layer M2 of the medulla, proximal to serotonergic boutons, suggesting that the medulla neuropil is the primary site of serotonergic regulation for these neurons. Exogenous serotonin increased basal intracellular calcium in L2 terminals in layer M2 and modestly decreased the duration of visually induced calcium transients in L2 neurons following repeated dark flashes, but otherwise did not alter the calcium transients. Flies without functional 5-HT2B failed to show an increase in basal calcium in response to serotonin. 5-HT2B mutants also failed to show a change in amplitude in their response to repeated light flashes but other calcium transient parameters were relatively unaffected. While we did not detect serotonin receptor expression in L1 neurons, they, like L2, underwent serotonin-induced changes in basal calcium, presumably via interactions with other cells. These data demonstrate that serotonin modulates the physiology of interneurons involved in early visual processing in Drosophila.

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“…5b). However, arguing against LC11 providing input to TSDNs is the finding that they are equally inhibited by background motion in the same as well as in the opposite direction to object motion 34 , inconsistent with TSDNs (Fig. 2).…”

Section: Discussionmentioning

confidence: 95%

“…This suggests that the target detection pathway receives inhibitory input from widefield motion. We assume that TSDNs receive input from STMDs 11,18 or other target tuned neurons 31,34-36 , potentially directly (dashed lines, pictograms, Fig. 5c, d).…”

Section: Resultsmentioning

confidence: 99%

Facilitation of neural responses to targets moving against optic flow

Nicholas

Nordström

2020

Preprint

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AbstractFor the human observer, it is difficult to follow the motion of small objects, especially when these are displayed against background motion. However, insects efficiently do this, as evidenced by their ability to capture prey, pursue conspecifics or defend territories, often in foliage-rich areas. This ability has been attributed to insect optic lobe neurons sharply tuned to target motion, as these respond robustly to targets even against moving backgrounds. However, their presumed post-synaptic counterparts, the target selective descending neurons (TSDNs), do not, suggesting inhibition by widefield motion. Importantly, though, previous experiments used panoramic background images, which not only lacked 3D cues, but also high-contrast features, experienced in natural flight. To mitigate this, we here use widefield motion consisting of many targets moving coherently to simulate the type of 3D optic flow that would be generated by the animal’s own motion through the world. We show that TSDNs are inhibited by syn-directional optic flow, consistent with previous findings. However, and more surprisingly, we show that TSDNs are facilitated by optic flow in the opposite direction to target motion. Our results thereby emphasize that the responses of descending neurons cannot simply be inferred from their presumed pre-synaptic counterparts.

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Inhibitory Interactions and Columnar Inputs to an Object Motion Detector in Drosophila

Cited by 42 publications

References 48 publications

Dragonfly visual neurons selectively attend to features in naturalistic scenes

Dragonfly visual neurons selectively attend to features in naturalistic scenes

Serotonergic modulation of visual neurons in Drosophila melanogaster

Facilitation of neural responses to targets moving against optic flow

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