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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

Lovebirds performed an intermittent flight style with two wingbeat distributions in which saccades are started during downstrokes.(A) The downstroke / upstroke phase ratio vs. instantaneous flap frequency distribution for individual wingbeats of five birds. A phase ratio of 1 indicates up- and downstrokes of equal duration, values <1 indicate longer upstrokes, values >1 longer downstrokes. Normalized bimodal Gaussian fits are shown for flap frequency (top) and for downstroke / upstroke time ratios (right). The bird-specific bimodal distribution parameters for the flapping frequency are: 2dg: μ1 = 9.78, σ1= 1.61, μ2 = 17.26, σ2= 1.01; 2lg: μ1 = 10.26, σ1= 1.83, μ2 = 18.14, σ2= 0.91; 2y: μ1 = 9.39, σ1= 1.1, μ2 = 17.19, σ2= 0.86; 1y: μ1 = 8.97, σ1= 0.6, μ2 = 15.76, σ2= 0.96; 3g: μ1 = 9.49, σ1= 2.3, μ2 = 16.72, σ2= 1; For downstroke / upstroke periods the obtained bimodal distribution parameters are: 2dg: μ1 = 0.5, σ1 = 0.07, μ2 = 1.26, σ2 = 0.27; 2lg: μ1 = 0.56, σ1 = 0.13, μ2 = 1.43, σ2 = 0.17; 2y: μ1 = 0.48, σ1 = 0.07, μ2 = 1.26, σ2 = 0.27; 1y: μ1 = 0.62, σ1 = 0.09, μ2 = 1.49, σ2 = 0.17; 3g: μ1 = 0.48, σ1 = 0.12, μ2 = 1.3, σ2 = 0.17. The horizontal gray line separates the bimodal distributions at a downstroke / upstroke ratio of 0.94 (average midpoint between bimodal distribution peaks among birds). The vertical gray line separates the bimodal distribution at a flap frequency of 13.3 Hz (average among birds); n = 697 wing beats, N = 5 birds. Due to the 2000 fps sample frequency, and the fact that wingbeat, downstroke, and upstroke time are all integer values measured in number of frames, the data appear in a raster and can overlap precisely among wings beats, flights and birds. (B) The normalized saccade distributions illustrate when a saccade was started and ended during the downstroke vs. the upstroke phase. Shown is the average across birds (solid lines) and the standard deviation (shaded area). Binning: 0:10:100; n = 72 saccades, N = 5 birds.
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pone.0129287.g003: Lovebirds performed an intermittent flight style with two wingbeat distributions in which saccades are started during downstrokes.(A) The downstroke / upstroke phase ratio vs. instantaneous flap frequency distribution for individual wingbeats of five birds. A phase ratio of 1 indicates up- and downstrokes of equal duration, values <1 indicate longer upstrokes, values >1 longer downstrokes. Normalized bimodal Gaussian fits are shown for flap frequency (top) and for downstroke / upstroke time ratios (right). The bird-specific bimodal distribution parameters for the flapping frequency are: 2dg: μ1 = 9.78, σ1= 1.61, μ2 = 17.26, σ2= 1.01; 2lg: μ1 = 10.26, σ1= 1.83, μ2 = 18.14, σ2= 0.91; 2y: μ1 = 9.39, σ1= 1.1, μ2 = 17.19, σ2= 0.86; 1y: μ1 = 8.97, σ1= 0.6, μ2 = 15.76, σ2= 0.96; 3g: μ1 = 9.49, σ1= 2.3, μ2 = 16.72, σ2= 1; For downstroke / upstroke periods the obtained bimodal distribution parameters are: 2dg: μ1 = 0.5, σ1 = 0.07, μ2 = 1.26, σ2 = 0.27; 2lg: μ1 = 0.56, σ1 = 0.13, μ2 = 1.43, σ2 = 0.17; 2y: μ1 = 0.48, σ1 = 0.07, μ2 = 1.26, σ2 = 0.27; 1y: μ1 = 0.62, σ1 = 0.09, μ2 = 1.49, σ2 = 0.17; 3g: μ1 = 0.48, σ1 = 0.12, μ2 = 1.3, σ2 = 0.17. The horizontal gray line separates the bimodal distributions at a downstroke / upstroke ratio of 0.94 (average midpoint between bimodal distribution peaks among birds). The vertical gray line separates the bimodal distribution at a flap frequency of 13.3 Hz (average among birds); n = 697 wing beats, N = 5 birds. Due to the 2000 fps sample frequency, and the fact that wingbeat, downstroke, and upstroke time are all integer values measured in number of frames, the data appear in a raster and can overlap precisely among wings beats, flights and birds. (B) The normalized saccade distributions illustrate when a saccade was started and ended during the downstroke vs. the upstroke phase. Shown is the average across birds (solid lines) and the standard deviation (shaded area). Binning: 0:10:100; n = 72 saccades, N = 5 birds.

Mentions: To give insight into how an actual recorded U-turn flight looks, we will illustrate one example first (Fig 2, S1 Movie) before presenting quantitative results across birds (Figs 3 to 7). In a typical recorded flight, the lovebird took off from the perch, flew more than halfway into the arena, performed a rapid turning maneuver ‘on a dime’ in which it oriented itself back to the perch, flew back to the perch and landed on it (Fig 2A).


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

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

Lovebirds performed an intermittent flight style with two wingbeat distributions in which saccades are started during downstrokes.(A) The downstroke / upstroke phase ratio vs. instantaneous flap frequency distribution for individual wingbeats of five birds. A phase ratio of 1 indicates up- and downstrokes of equal duration, values <1 indicate longer upstrokes, values >1 longer downstrokes. Normalized bimodal Gaussian fits are shown for flap frequency (top) and for downstroke / upstroke time ratios (right). The bird-specific bimodal distribution parameters for the flapping frequency are: 2dg: μ1 = 9.78, σ1= 1.61, μ2 = 17.26, σ2= 1.01; 2lg: μ1 = 10.26, σ1= 1.83, μ2 = 18.14, σ2= 0.91; 2y: μ1 = 9.39, σ1= 1.1, μ2 = 17.19, σ2= 0.86; 1y: μ1 = 8.97, σ1= 0.6, μ2 = 15.76, σ2= 0.96; 3g: μ1 = 9.49, σ1= 2.3, μ2 = 16.72, σ2= 1; For downstroke / upstroke periods the obtained bimodal distribution parameters are: 2dg: μ1 = 0.5, σ1 = 0.07, μ2 = 1.26, σ2 = 0.27; 2lg: μ1 = 0.56, σ1 = 0.13, μ2 = 1.43, σ2 = 0.17; 2y: μ1 = 0.48, σ1 = 0.07, μ2 = 1.26, σ2 = 0.27; 1y: μ1 = 0.62, σ1 = 0.09, μ2 = 1.49, σ2 = 0.17; 3g: μ1 = 0.48, σ1 = 0.12, μ2 = 1.3, σ2 = 0.17. The horizontal gray line separates the bimodal distributions at a downstroke / upstroke ratio of 0.94 (average midpoint between bimodal distribution peaks among birds). The vertical gray line separates the bimodal distribution at a flap frequency of 13.3 Hz (average among birds); n = 697 wing beats, N = 5 birds. Due to the 2000 fps sample frequency, and the fact that wingbeat, downstroke, and upstroke time are all integer values measured in number of frames, the data appear in a raster and can overlap precisely among wings beats, flights and birds. (B) The normalized saccade distributions illustrate when a saccade was started and ended during the downstroke vs. the upstroke phase. Shown is the average across birds (solid lines) and the standard deviation (shaded area). Binning: 0:10:100; n = 72 saccades, N = 5 birds.
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pone.0129287.g003: Lovebirds performed an intermittent flight style with two wingbeat distributions in which saccades are started during downstrokes.(A) The downstroke / upstroke phase ratio vs. instantaneous flap frequency distribution for individual wingbeats of five birds. A phase ratio of 1 indicates up- and downstrokes of equal duration, values <1 indicate longer upstrokes, values >1 longer downstrokes. Normalized bimodal Gaussian fits are shown for flap frequency (top) and for downstroke / upstroke time ratios (right). The bird-specific bimodal distribution parameters for the flapping frequency are: 2dg: μ1 = 9.78, σ1= 1.61, μ2 = 17.26, σ2= 1.01; 2lg: μ1 = 10.26, σ1= 1.83, μ2 = 18.14, σ2= 0.91; 2y: μ1 = 9.39, σ1= 1.1, μ2 = 17.19, σ2= 0.86; 1y: μ1 = 8.97, σ1= 0.6, μ2 = 15.76, σ2= 0.96; 3g: μ1 = 9.49, σ1= 2.3, μ2 = 16.72, σ2= 1; For downstroke / upstroke periods the obtained bimodal distribution parameters are: 2dg: μ1 = 0.5, σ1 = 0.07, μ2 = 1.26, σ2 = 0.27; 2lg: μ1 = 0.56, σ1 = 0.13, μ2 = 1.43, σ2 = 0.17; 2y: μ1 = 0.48, σ1 = 0.07, μ2 = 1.26, σ2 = 0.27; 1y: μ1 = 0.62, σ1 = 0.09, μ2 = 1.49, σ2 = 0.17; 3g: μ1 = 0.48, σ1 = 0.12, μ2 = 1.3, σ2 = 0.17. The horizontal gray line separates the bimodal distributions at a downstroke / upstroke ratio of 0.94 (average midpoint between bimodal distribution peaks among birds). The vertical gray line separates the bimodal distribution at a flap frequency of 13.3 Hz (average among birds); n = 697 wing beats, N = 5 birds. Due to the 2000 fps sample frequency, and the fact that wingbeat, downstroke, and upstroke time are all integer values measured in number of frames, the data appear in a raster and can overlap precisely among wings beats, flights and birds. (B) The normalized saccade distributions illustrate when a saccade was started and ended during the downstroke vs. the upstroke phase. Shown is the average across birds (solid lines) and the standard deviation (shaded area). Binning: 0:10:100; n = 72 saccades, N = 5 birds.
Mentions: To give insight into how an actual recorded U-turn flight looks, we will illustrate one example first (Fig 2, S1 Movie) before presenting quantitative results across birds (Figs 3 to 7). In a typical recorded flight, the lovebird took off from the perch, flew more than halfway into the arena, performed a rapid turning maneuver ‘on a dime’ in which it oriented itself back to the perch, flew back to the perch and landed on it (Fig 2A).

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