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How Lovebirds Maneuver Rapidly Using Super-Fast Head Saccades and Image Feature Stabilization.

Kress D, van Bokhorst E, Lentink D - PLoS ONE (2015)

Bottom Line: High-speed flight recordings revealed that rapidly turning lovebirds perform a remarkable stereotypical gaze behavior with peak saccadic head turns up to 2700 degrees per second, as fast as insects, enabled by fast neck muscles.Similarly, before landing, the lovebirds stabilize the center of the perch in their visual midline.Similar gaze behaviors have been reported for visually navigating humans.

View Article: PubMed Central - PubMed

Affiliation: Department of Mechanical Engineering, Stanford University, Stanford, California, United States of America.

ABSTRACT
Diurnal flying animals such as birds depend primarily on vision to coordinate their flight path during goal-directed flight tasks. To extract the spatial structure of the surrounding environment, birds are thought to use retinal image motion (optical flow) that is primarily induced by motion of their head. It is unclear what gaze behaviors birds perform to support visuomotor control during rapid maneuvering flight in which they continuously switch between flight modes. To analyze this, we measured the gaze behavior of rapidly turning lovebirds in a goal-directed task: take-off and fly away from a perch, turn on a dime, and fly back and land on the same perch. High-speed flight recordings revealed that rapidly turning lovebirds perform a remarkable stereotypical gaze behavior with peak saccadic head turns up to 2700 degrees per second, as fast as insects, enabled by fast neck muscles. In between saccades, gaze orientation is held constant. By comparing saccade and wingbeat phase, we find that these super-fast saccades are coordinated with the downstroke when the lateral visual field is occluded by the wings. Lovebirds thus maximize visual perception by overlying behaviors that impair vision, which helps coordinate maneuvers. Before the turn, lovebirds keep a high contrast edge in their visual midline. Similarly, before landing, the lovebirds stabilize the center of the perch in their visual midline. The perch on which the birds land swings, like a branch in the wind, and we find that retinal size of the perch is the most parsimonious visual cue to initiate landing. Our observations show that rapidly maneuvering birds use precisely timed stereotypic gaze behaviors consisting of rapid head turns and frontal feature stabilization, which facilitates optical flow based flight control. Similar gaze behaviors have been reported for visually navigating humans. This finding can inspire more effective vision-based autopilots for drones.

No MeSH data available.


Related in: MedlinePlus

Individual example of a turning on a dime maneuver.(A) Head trajectory during a leftward U-turn flight maneuver in the flight arena. Plotted head position (gray dots) and head yaw orientation (red lines) are presented in 25 ms steps (50 frames). Because the turn is performed on a dime, traces after takeoff and before landing overlap. Arena wall grayscale (black, gray, and white) illustrates the inner wall texture seen by the bird. The thick black bar in the arena shows the perch position. (B) Top view of all 15 wing-tip positions at mid stroke during the same turn maneuver as shown in (A). Deflections in wing tip traces (wing beat 5–6 & 11–12) were used to separate the continuous flight maneuver into three consecutive phases: before turn (gray), during turn (blue) and after turn (red). (C) Head (red) and body (blue) yaw orientation angle (Φ) during a left turn maneuver. Φ is calculated in relation to a horizontal axis in the flight arena (see Fig 1 and methods). Φ values of 0° indicate an orientation along the horizontal axis facing away from the perch whereas Φ of 180° indicates an orientation along this axis facing towards the perch. Positive Φ deflections indicate a turn to the left, negative ones a turn to the right. The Φ difference angle between head and body is shown in green. Body data was filtered and interpolated (blue dashed line, see methods) to calculate the Φ head-body angle. Vertical bars represent the downstroke phases and thereby the wing beat timing before, during and after the turn. (D) Saccade detection (black, see text) based on absolute yaw rotation velocity (ω, gray graph). The dashed gray line illustrates the saccade detection threshold of 400°/s that ω had to exceed for at least 12 ms (24 data points) to define a head turn as saccadic.
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pone.0129287.g002: Individual example of a turning on a dime maneuver.(A) Head trajectory during a leftward U-turn flight maneuver in the flight arena. Plotted head position (gray dots) and head yaw orientation (red lines) are presented in 25 ms steps (50 frames). Because the turn is performed on a dime, traces after takeoff and before landing overlap. Arena wall grayscale (black, gray, and white) illustrates the inner wall texture seen by the bird. The thick black bar in the arena shows the perch position. (B) Top view of all 15 wing-tip positions at mid stroke during the same turn maneuver as shown in (A). Deflections in wing tip traces (wing beat 5–6 & 11–12) were used to separate the continuous flight maneuver into three consecutive phases: before turn (gray), during turn (blue) and after turn (red). (C) Head (red) and body (blue) yaw orientation angle (Φ) during a left turn maneuver. Φ is calculated in relation to a horizontal axis in the flight arena (see Fig 1 and methods). Φ values of 0° indicate an orientation along the horizontal axis facing away from the perch whereas Φ of 180° indicates an orientation along this axis facing towards the perch. Positive Φ deflections indicate a turn to the left, negative ones a turn to the right. The Φ difference angle between head and body is shown in green. Body data was filtered and interpolated (blue dashed line, see methods) to calculate the Φ head-body angle. Vertical bars represent the downstroke phases and thereby the wing beat timing before, during and after the turn. (D) Saccade detection (black, see text) based on absolute yaw rotation velocity (ω, gray graph). The dashed gray line illustrates the saccade detection threshold of 400°/s that ω had to exceed for at least 12 ms (24 data points) to define a head turn as saccadic.

Mentions: One of the arena’s inner sidewalls was covered with a white cardboard sheet over the full length. This white wall had a small grey textured rectangle measuring 25 cm x 20 cm positioned at its center (Fig 1A). The arena floor was covered with plastic film to increase the birds’ contrast on the video images. As the illuminated flight arena was placed in a completely darkened room, all its walls except one sidewall appeared black to birds within it. Consequently, wall edges between the white and the dark walls constitute features with strong contrast within the arena. To film the flying bird from above, two laterally placed high-speed cameras (Photron APX and PCI camera, Photron Inc, San Diego, CA, USA) were directed at an inclined mirror above the arena (Fig 1A). For orientation reference: in the following sections, we will describe our findings based on the recorded camera images which are mirrored around the horizontal axis—thus right and left arena sides are switched. Consequently, when mentioning the white sidewall appearing left in our figures (Figs 1C and 2A), we are actually describing the right arena sidewall (see Fig 1A & 1C for clarification). The same holds for turning directions (S1 Movie).


How Lovebirds Maneuver Rapidly Using Super-Fast Head Saccades and Image Feature Stabilization.

Kress D, van Bokhorst E, Lentink D - PLoS ONE (2015)

Individual example of a turning on a dime maneuver.(A) Head trajectory during a leftward U-turn flight maneuver in the flight arena. Plotted head position (gray dots) and head yaw orientation (red lines) are presented in 25 ms steps (50 frames). Because the turn is performed on a dime, traces after takeoff and before landing overlap. Arena wall grayscale (black, gray, and white) illustrates the inner wall texture seen by the bird. The thick black bar in the arena shows the perch position. (B) Top view of all 15 wing-tip positions at mid stroke during the same turn maneuver as shown in (A). Deflections in wing tip traces (wing beat 5–6 & 11–12) were used to separate the continuous flight maneuver into three consecutive phases: before turn (gray), during turn (blue) and after turn (red). (C) Head (red) and body (blue) yaw orientation angle (Φ) during a left turn maneuver. Φ is calculated in relation to a horizontal axis in the flight arena (see Fig 1 and methods). Φ values of 0° indicate an orientation along the horizontal axis facing away from the perch whereas Φ of 180° indicates an orientation along this axis facing towards the perch. Positive Φ deflections indicate a turn to the left, negative ones a turn to the right. The Φ difference angle between head and body is shown in green. Body data was filtered and interpolated (blue dashed line, see methods) to calculate the Φ head-body angle. Vertical bars represent the downstroke phases and thereby the wing beat timing before, during and after the turn. (D) Saccade detection (black, see text) based on absolute yaw rotation velocity (ω, gray graph). The dashed gray line illustrates the saccade detection threshold of 400°/s that ω had to exceed for at least 12 ms (24 data points) to define a head turn as saccadic.
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Related In: Results  -  Collection

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Show All Figures
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pone.0129287.g002: Individual example of a turning on a dime maneuver.(A) Head trajectory during a leftward U-turn flight maneuver in the flight arena. Plotted head position (gray dots) and head yaw orientation (red lines) are presented in 25 ms steps (50 frames). Because the turn is performed on a dime, traces after takeoff and before landing overlap. Arena wall grayscale (black, gray, and white) illustrates the inner wall texture seen by the bird. The thick black bar in the arena shows the perch position. (B) Top view of all 15 wing-tip positions at mid stroke during the same turn maneuver as shown in (A). Deflections in wing tip traces (wing beat 5–6 & 11–12) were used to separate the continuous flight maneuver into three consecutive phases: before turn (gray), during turn (blue) and after turn (red). (C) Head (red) and body (blue) yaw orientation angle (Φ) during a left turn maneuver. Φ is calculated in relation to a horizontal axis in the flight arena (see Fig 1 and methods). Φ values of 0° indicate an orientation along the horizontal axis facing away from the perch whereas Φ of 180° indicates an orientation along this axis facing towards the perch. Positive Φ deflections indicate a turn to the left, negative ones a turn to the right. The Φ difference angle between head and body is shown in green. Body data was filtered and interpolated (blue dashed line, see methods) to calculate the Φ head-body angle. Vertical bars represent the downstroke phases and thereby the wing beat timing before, during and after the turn. (D) Saccade detection (black, see text) based on absolute yaw rotation velocity (ω, gray graph). The dashed gray line illustrates the saccade detection threshold of 400°/s that ω had to exceed for at least 12 ms (24 data points) to define a head turn as saccadic.
Mentions: One of the arena’s inner sidewalls was covered with a white cardboard sheet over the full length. This white wall had a small grey textured rectangle measuring 25 cm x 20 cm positioned at its center (Fig 1A). The arena floor was covered with plastic film to increase the birds’ contrast on the video images. As the illuminated flight arena was placed in a completely darkened room, all its walls except one sidewall appeared black to birds within it. Consequently, wall edges between the white and the dark walls constitute features with strong contrast within the arena. To film the flying bird from above, two laterally placed high-speed cameras (Photron APX and PCI camera, Photron Inc, San Diego, CA, USA) were directed at an inclined mirror above the arena (Fig 1A). For orientation reference: in the following sections, we will describe our findings based on the recorded camera images which are mirrored around the horizontal axis—thus right and left arena sides are switched. Consequently, when mentioning the white sidewall appearing left in our figures (Figs 1C and 2A), we are actually describing the right arena sidewall (see Fig 1A & 1C for clarification). The same holds for turning directions (S1 Movie).

Bottom Line: High-speed flight recordings revealed that rapidly turning lovebirds perform a remarkable stereotypical gaze behavior with peak saccadic head turns up to 2700 degrees per second, as fast as insects, enabled by fast neck muscles.Similarly, before landing, the lovebirds stabilize the center of the perch in their visual midline.Similar gaze behaviors have been reported for visually navigating humans.

View Article: PubMed Central - PubMed

Affiliation: Department of Mechanical Engineering, Stanford University, Stanford, California, United States of America.

ABSTRACT
Diurnal flying animals such as birds depend primarily on vision to coordinate their flight path during goal-directed flight tasks. To extract the spatial structure of the surrounding environment, birds are thought to use retinal image motion (optical flow) that is primarily induced by motion of their head. It is unclear what gaze behaviors birds perform to support visuomotor control during rapid maneuvering flight in which they continuously switch between flight modes. To analyze this, we measured the gaze behavior of rapidly turning lovebirds in a goal-directed task: take-off and fly away from a perch, turn on a dime, and fly back and land on the same perch. High-speed flight recordings revealed that rapidly turning lovebirds perform a remarkable stereotypical gaze behavior with peak saccadic head turns up to 2700 degrees per second, as fast as insects, enabled by fast neck muscles. In between saccades, gaze orientation is held constant. By comparing saccade and wingbeat phase, we find that these super-fast saccades are coordinated with the downstroke when the lateral visual field is occluded by the wings. Lovebirds thus maximize visual perception by overlying behaviors that impair vision, which helps coordinate maneuvers. Before the turn, lovebirds keep a high contrast edge in their visual midline. Similarly, before landing, the lovebirds stabilize the center of the perch in their visual midline. The perch on which the birds land swings, like a branch in the wind, and we find that retinal size of the perch is the most parsimonious visual cue to initiate landing. Our observations show that rapidly maneuvering birds use precisely timed stereotypic gaze behaviors consisting of rapid head turns and frontal feature stabilization, which facilitates optical flow based flight control. Similar gaze behaviors have been reported for visually navigating humans. This finding can inspire more effective vision-based autopilots for drones.

No MeSH data available.


Related in: MedlinePlus