Walking Modulates Speed Sensitivity in Drosophila Motion Vision

Chiappe, M. Eugenia; Seelig, Johannes D.; Reiser, Michael B.; Jayaraman, Vivek

doi:10.1016/j.cub.2010.06.072

Cited by 269 publications

(289 citation statements)

References 41 publications

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“…In agreement with previous work (31,33), HSN in the left lobula plate (Fig. 3B) responded to standard motion in its preferred or counter clockwise (CCW) direction with an increase in calcium signal.…”

Section: Resultssupporting

confidence: 93%

Neural correlates of illusory motion perception in Drosophila

Tuthill

Chiappe

Reiser

2011

Proc. Natl. Acad. Sci. U.S.A.

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When the contrast of an image flickers as it moves, humans perceive an illusory reversal in the direction of motion. This classic illusion, called reverse-phi motion, has been well-characterized using psychophysics, and several models have been proposed to account for its effects. Here, we show that Drosophila melanogaster also respond behaviorally to the reverse-phi illusion and that the illusion is present in dendritic calcium signals of motion-sensitive neurons in the fly lobula plate. These results closely match the predictions of the predominant model of fly motion detection. However, high flicker rates cause an inversion of the reverse-phi behavioral response that is also present in calcium signals of lobula plate tangential cell dendrites but not predicted by the model. The fly's behavioral and neural responses to the reverse-phi illusion reveal unexpected interactions between motion and flicker signals in the fly visual system and suggest that a similar correlation-based mechanism underlies visual motion detection across the animal kingdom.fly vision | Drosophila behavior | calcium imaging | visual illusion A mong visual organisms, the ability to detect motion is nearly universal. Animals as diverse as weevils (1) and wallabies (2) compute visual motion from time-varying patterns of brightness received by an array of photoreceptors. However, the mechanisms by which the visual system detects motion are not wellunderstood in any animal (3). Here, we use a visual illusion to probe the mechanisms of motion detection in the fly, Drosophila melanogaster.Sequential flashes at neighboring spatial positions cause humans to perceive motion in the direction of the second flash, an effect called phi or apparent motion (4). A related phenomenon, reverse-phi motion, also relies on sequential luminance changes to evoke a motion percept (5); however, in the reverse-phi stimulus, the contrast polarity of the stimulus inverts as it moves, causing a reversal in the direction of perceived motion (Movie S1). For example, when a black random dot pattern turns to white as it moves right across a gray background, human subjects perceive left motion (6).The reverse-phi effect is not a subtle illusion. Humans exhibit nearly equal sensitivity and comparable spatial and temporal tuning for standard and reverse-phi motion (7). Sensitivity to reverse-phi has also been shown for other vertebrates such as primates (8) and zebrafish (9). Directional responses to reversephi motion are present in cat striate cortex (10), the nucleus of the optic tract in the wallaby (2), and the middle temporal area (MT) of primate visual cortex (8, 11). These psychophysical and neurophysiological data suggest that sensitivity to reverse-phi motion may be a common feature of motion detection in the vertebrate visual system, and for this reason, reverse-phi has been an important tool for building models of visual motion detection (8,(12)(13)(14)(15)(16).The prevailing simple model for motion detection in the fly is the Hassenstein-Reichardt elementary moti...

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Section: Resultssupporting

confidence: 93%

Neural correlates of illusory motion perception in Drosophila

Tuthill

Chiappe

Reiser

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…Therefore, the additional increase in fire rate might have been occluded due to output saturation. Maimon et al (2010) and Chiappe et al (2010) found an increase in the response of LPTCs of moving compared with nonmoving Drosophila. Furthermore, Chiappe et al (2010) demonstrated a shift of the temporal frequency optimum from 1 to 3 Hz in walking Drosophila.…”

Section: Discussionmentioning

confidence: 95%

“…In these studies, it was shown that the response gain of lobula plate tangential cells in Drosophila is enhanced during locomotion (Chiappe et al, 2010;Maimon et al, 2010). In addition, Chiappe et al (2010) demonstrated that during walking, the peak of the velocity tuning of the cells of the horizontal system is shifted toward higher velocities compared with resting flies. For the reasons outlined above, velocity tuning might even be altered more strongly when flying instead of walking.…”

Section: Introductionmentioning

confidence: 99%

“…Given how different the tasks of passively receiving a stimulus and active sensation are, it is not surprising that this assumption has been challenged more recently. Several pioneering studies, in vertebrates as well as insects, demonstrated that the behavioral state of an animal has a strong influence on sensory processing (Treue and Maunsell, 1996;Rind et al, 2008;Chiappe et al, 2010;Haag et al, 2010;Maimon et al, 2010;Niell and Stryker, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Flight Activity Alters Velocity Tuning of Fly Motion-Sensitive Neurons

Jung¹,

Borst²,

Haag³

2011

Journal of Neuroscience

114

141

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Sensory neurons are mostly studied in fixed animals, but their response properties might change when the animal is free to move. Indeed, recent studies found differences between responses of sensory neurons in resting versus moving insects. Since the dynamic range of visual motion stimuli strongly depends on the speed at which an animal is moving, we investigated whether the visual system adapts to such changes in stimulus dynamics as induced by self-motion. Lobula plate tangential cells of flies lend themselves well to study this question because they are known to code for ego-motion based on optic-flow. We recorded the responses of the lobula plate tangential cell H1 to a visual pattern moving at different velocities under three different conditions: fixed flies before and after application of the octopamine agonist chlordimeform (CDM) and tethered flying flies. CDM has been previously shown to induce arousal in flies. We found that flying as well as the application of CDM significantly broadens the velocity tuning of H1 toward higher velocities.

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“…These studies have revealed frequency optima around 1 Hz for stationary Drosophila, Phaenicia, and Calliphora (see Joesch et al 2008;Eckert 1980;Haag et al 2004, respectively). For walking Drosophila optima from 2 to 3 Hz have been shown (Götz and Wenking 1973;Chiappe et al 2010). In flying animals, optima have been reported between 3 and 10 Hz for Drosophila (Duistermars et al 2007;Fry et al 2009), 1 to 10 Hz for Musca (Borst and Bahde 1987) and 5 to 7 Hz for Calliphora (Hausen and Wehrhahn 1989;Jung et al 2011).…”

Section: Emd Output Characteristicsmentioning

confidence: 94%

Bio-inspired visual ego-rotation sensor for MAVs

et al. 2012

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Flies are capable of extraordinary flight maneuvers at very high speeds largely due to their highly elaborate visual system. In this work we present a fly-inspired FPGA based sensor system able to visually sense rotations around different body axes, for use on board micro aerial vehicles (MAVs). Rotation sensing is performed analogously to the fly's VS cell network using zero-crossing detection. An additional key feature of our system is the ease of adding new functionalities akin to the different tasks attributed to the fly's lobula plate tangential cell network, such as object avoidance or collision detection. Our implementation consists of a modified eneo SC-MVC01 SmartCam module and a custom built circuit board, weighing less than 200 g and consuming less than 4 W while featuring 57,600 individual two-dimensional elementary motion detectors, a 185 • field of view and a frame rate of 350 frames per second. This makes our sensor system compact in terms of size, weight and power requirements for easy incorporation into MAV platforms, while autonomously performing all sensing and processing on-board and in real time.

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Walking Modulates Speed Sensitivity in Drosophila Motion Vision

Cited by 269 publications

References 41 publications

Neural correlates of illusory motion perception in Drosophila

Neural correlates of illusory motion perception in Drosophila

Flight Activity Alters Velocity Tuning of Fly Motion-Sensitive Neurons

Bio-inspired visual ego-rotation sensor for MAVs

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