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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

Distributions of intersaccadic azimuthal feature positions reveal that maneuvering birds stabilize arena features in their frontal visual field.(A) Schematic top view into the arena. Azimuthal positions of wall corners, the gray square and the perch (colored lines) were obtained relative to the bird’s head yaw orientation (red line). (B) Relative azimuthal angles of arena features for the example flight shown in Fig 2. The thick green line depicts the angle of the perch center. The gray shaded area represents feasible horizontal eye motions of ±10° relative to the horizontal head orientation. Positive azimuthal angles represent the left visual hemisphere, negative values the right visual hemisphere (see bird illustration above legend). Note that the diverging azimuthal angles of the perch edges (dark green and blue lines) are caused by the bird getting closer to the perch. Approaching the perch causes the retinal size of the perch to expand in the bird’s frontal visual field. (C-F) Averaged relative azimuthal distributions of arena features that were stabilized in the frontal visual field in the intersaccadic phases during a turning on a dime maneuver; before the turn (C: fine dashed line), during the turn (D & E: solid line) and after turning (F: coarse dashed line). Averaged distributions illustrate left turn flights (n = 92, N = 5). Standard deviations across birds are illustrated by the colored areas. (G-K) Intersaccadic azimuthal distributions for arena features that were not stabilized in the frontal visual field. By stabilizing the perch center frontally after the turn (F), the right and left edge distributions are positioned more laterally, are broader and have lower peaks than the center (E & K). The vertical bar extending ±10° illustrates feasible horizontal eye motions relative to the head orientation in unrestricted birds (review: [14]). Perch position for 92 flights is approximated by using the position of a static perch (thick lines in panel E-F, n = 92 flights, N = 5). For 15 left-turn-flights tracked at 2000 Hz, the position of the swinging perch relative to the birds was tracked as well (gray dashed line in panel E, F & K n = 15 flights, N = 5). For normalization, we divided each distribution by the cumulative sum of all other feature distributions. Binning = -90:10:90.
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pone.0129287.g006: Distributions of intersaccadic azimuthal feature positions reveal that maneuvering birds stabilize arena features in their frontal visual field.(A) Schematic top view into the arena. Azimuthal positions of wall corners, the gray square and the perch (colored lines) were obtained relative to the bird’s head yaw orientation (red line). (B) Relative azimuthal angles of arena features for the example flight shown in Fig 2. The thick green line depicts the angle of the perch center. The gray shaded area represents feasible horizontal eye motions of ±10° relative to the horizontal head orientation. Positive azimuthal angles represent the left visual hemisphere, negative values the right visual hemisphere (see bird illustration above legend). Note that the diverging azimuthal angles of the perch edges (dark green and blue lines) are caused by the bird getting closer to the perch. Approaching the perch causes the retinal size of the perch to expand in the bird’s frontal visual field. (C-F) Averaged relative azimuthal distributions of arena features that were stabilized in the frontal visual field in the intersaccadic phases during a turning on a dime maneuver; before the turn (C: fine dashed line), during the turn (D & E: solid line) and after turning (F: coarse dashed line). Averaged distributions illustrate left turn flights (n = 92, N = 5). Standard deviations across birds are illustrated by the colored areas. (G-K) Intersaccadic azimuthal distributions for arena features that were not stabilized in the frontal visual field. By stabilizing the perch center frontally after the turn (F), the right and left edge distributions are positioned more laterally, are broader and have lower peaks than the center (E & K). The vertical bar extending ±10° illustrates feasible horizontal eye motions relative to the head orientation in unrestricted birds (review: [14]). Perch position for 92 flights is approximated by using the position of a static perch (thick lines in panel E-F, n = 92 flights, N = 5). For 15 left-turn-flights tracked at 2000 Hz, the position of the swinging perch relative to the birds was tracked as well (gray dashed line in panel E, F & K n = 15 flights, N = 5). For normalization, we divided each distribution by the cumulative sum of all other feature distributions. Binning = -90:10:90.

Mentions: By combining head orientation and flight arena geometry (Fig 6A), we found that maneuvering lovebirds stabilize high contrast features in their frontal visual field during intersaccades. Therefore, we indicate the range of feasible eye movements, which results in an uncertainty in the estimated gaze direction in the frontal visual field, using a gray horizontal bar in Fig 6B and Fig 6C–6K. Typical gaze shifts (based on Fig 2) are shown in Fig 6B. To analyze gaze distributions quantitatively, we averaged retinal feature positions across birds (n = 92, N = 5) [21]. Due to motion blur [36] and saccadic suppression [34,35], we focused our quantitative gaze analysis on intersaccadic phases for which head orientation is relatively constant (Figs 2D and 4D). We investigated these phases across 92 left turn flights (including the 15 left turns resolved at 2000 Hz) for which we then tracked the head at four times the wingbeat frequency (about 68 Hz). To separate saccadic from intersaccadic phases in this larger data set, Fig 4A, we excluded head yaw data which exceeded a standard deviation of 10° yaw per wingbeat (± 10°: gray shaded bar in Fig 6B–6K, [13–15]). This value is based on the largest horizontal eye movements that may assist in stabilizing gaze. Azimuthal angle distributions were independent of acquisition rate (correlation coefficients for compared arena features > 0.9). Hence, lower temporal resolution wingbeat data can be used robustly to determine intersaccadic head orientation.


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

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

Distributions of intersaccadic azimuthal feature positions reveal that maneuvering birds stabilize arena features in their frontal visual field.(A) Schematic top view into the arena. Azimuthal positions of wall corners, the gray square and the perch (colored lines) were obtained relative to the bird’s head yaw orientation (red line). (B) Relative azimuthal angles of arena features for the example flight shown in Fig 2. The thick green line depicts the angle of the perch center. The gray shaded area represents feasible horizontal eye motions of ±10° relative to the horizontal head orientation. Positive azimuthal angles represent the left visual hemisphere, negative values the right visual hemisphere (see bird illustration above legend). Note that the diverging azimuthal angles of the perch edges (dark green and blue lines) are caused by the bird getting closer to the perch. Approaching the perch causes the retinal size of the perch to expand in the bird’s frontal visual field. (C-F) Averaged relative azimuthal distributions of arena features that were stabilized in the frontal visual field in the intersaccadic phases during a turning on a dime maneuver; before the turn (C: fine dashed line), during the turn (D & E: solid line) and after turning (F: coarse dashed line). Averaged distributions illustrate left turn flights (n = 92, N = 5). Standard deviations across birds are illustrated by the colored areas. (G-K) Intersaccadic azimuthal distributions for arena features that were not stabilized in the frontal visual field. By stabilizing the perch center frontally after the turn (F), the right and left edge distributions are positioned more laterally, are broader and have lower peaks than the center (E & K). The vertical bar extending ±10° illustrates feasible horizontal eye motions relative to the head orientation in unrestricted birds (review: [14]). Perch position for 92 flights is approximated by using the position of a static perch (thick lines in panel E-F, n = 92 flights, N = 5). For 15 left-turn-flights tracked at 2000 Hz, the position of the swinging perch relative to the birds was tracked as well (gray dashed line in panel E, F & K n = 15 flights, N = 5). For normalization, we divided each distribution by the cumulative sum of all other feature distributions. Binning = -90:10:90.
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pone.0129287.g006: Distributions of intersaccadic azimuthal feature positions reveal that maneuvering birds stabilize arena features in their frontal visual field.(A) Schematic top view into the arena. Azimuthal positions of wall corners, the gray square and the perch (colored lines) were obtained relative to the bird’s head yaw orientation (red line). (B) Relative azimuthal angles of arena features for the example flight shown in Fig 2. The thick green line depicts the angle of the perch center. The gray shaded area represents feasible horizontal eye motions of ±10° relative to the horizontal head orientation. Positive azimuthal angles represent the left visual hemisphere, negative values the right visual hemisphere (see bird illustration above legend). Note that the diverging azimuthal angles of the perch edges (dark green and blue lines) are caused by the bird getting closer to the perch. Approaching the perch causes the retinal size of the perch to expand in the bird’s frontal visual field. (C-F) Averaged relative azimuthal distributions of arena features that were stabilized in the frontal visual field in the intersaccadic phases during a turning on a dime maneuver; before the turn (C: fine dashed line), during the turn (D & E: solid line) and after turning (F: coarse dashed line). Averaged distributions illustrate left turn flights (n = 92, N = 5). Standard deviations across birds are illustrated by the colored areas. (G-K) Intersaccadic azimuthal distributions for arena features that were not stabilized in the frontal visual field. By stabilizing the perch center frontally after the turn (F), the right and left edge distributions are positioned more laterally, are broader and have lower peaks than the center (E & K). The vertical bar extending ±10° illustrates feasible horizontal eye motions relative to the head orientation in unrestricted birds (review: [14]). Perch position for 92 flights is approximated by using the position of a static perch (thick lines in panel E-F, n = 92 flights, N = 5). For 15 left-turn-flights tracked at 2000 Hz, the position of the swinging perch relative to the birds was tracked as well (gray dashed line in panel E, F & K n = 15 flights, N = 5). For normalization, we divided each distribution by the cumulative sum of all other feature distributions. Binning = -90:10:90.
Mentions: By combining head orientation and flight arena geometry (Fig 6A), we found that maneuvering lovebirds stabilize high contrast features in their frontal visual field during intersaccades. Therefore, we indicate the range of feasible eye movements, which results in an uncertainty in the estimated gaze direction in the frontal visual field, using a gray horizontal bar in Fig 6B and Fig 6C–6K. Typical gaze shifts (based on Fig 2) are shown in Fig 6B. To analyze gaze distributions quantitatively, we averaged retinal feature positions across birds (n = 92, N = 5) [21]. Due to motion blur [36] and saccadic suppression [34,35], we focused our quantitative gaze analysis on intersaccadic phases for which head orientation is relatively constant (Figs 2D and 4D). We investigated these phases across 92 left turn flights (including the 15 left turns resolved at 2000 Hz) for which we then tracked the head at four times the wingbeat frequency (about 68 Hz). To separate saccadic from intersaccadic phases in this larger data set, Fig 4A, we excluded head yaw data which exceeded a standard deviation of 10° yaw per wingbeat (± 10°: gray shaded bar in Fig 6B–6K, [13–15]). This value is based on the largest horizontal eye movements that may assist in stabilizing gaze. Azimuthal angle distributions were independent of acquisition rate (correlation coefficients for compared arena features > 0.9). Hence, lower temporal resolution wingbeat data can be used robustly to determine intersaccadic head orientation.

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