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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

Lovebird head rotation is predominantly saccadic at the highest average speed recorded amongst vertebrates.(A) Comparison of horizontal saccade amplitude as a function of its duration. Shown are saccade amplitudes and durations measured in this study (blue triangles, n = 72, N = 5) and data for other species extracted from earlier publications. Gray triangle markers represent the combined eye-head gaze shifts of rhesus macaques (n = 544, N = 2) [30]. Red, green and violet circles illustrate horizontal eye saccades in humans (n = 187, N = 3) [31], rabbits (n = 191, N = 2) [33] and cats (n = 34, N = 2) [32]. We coarsely approximate average head rotation velocities by fitting the data with a linear regression. Line equations: lovebird: y = 1.5*x-14, slope = 1500°/s, R2 = 0.78; rhesus macaque y = 0.4*x+3.4, slope = 400°/s, R2 = 0.69; human: 0.38*x+3.4, slope = 380°/s, R2 = 0.93; rabbit: y = 0.33*x-10, slope = 260°/s, R2 = 0.67, cat: y = 0.11*x-4.2, slope = 110°/s, R2 = 0.81. (B) Proportion of saccadic turns on the whole U-turn maneuver. Shown is the average cumulative saccade amplitude (and standard deviation) as a percentage of the whole turn amplitude, with the red line showing the average across birds (n = 72 saccades, N = 5 birds).
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pone.0129287.g005: Lovebird head rotation is predominantly saccadic at the highest average speed recorded amongst vertebrates.(A) Comparison of horizontal saccade amplitude as a function of its duration. Shown are saccade amplitudes and durations measured in this study (blue triangles, n = 72, N = 5) and data for other species extracted from earlier publications. Gray triangle markers represent the combined eye-head gaze shifts of rhesus macaques (n = 544, N = 2) [30]. Red, green and violet circles illustrate horizontal eye saccades in humans (n = 187, N = 3) [31], rabbits (n = 191, N = 2) [33] and cats (n = 34, N = 2) [32]. We coarsely approximate average head rotation velocities by fitting the data with a linear regression. Line equations: lovebird: y = 1.5*x-14, slope = 1500°/s, R2 = 0.78; rhesus macaque y = 0.4*x+3.4, slope = 400°/s, R2 = 0.69; human: 0.38*x+3.4, slope = 380°/s, R2 = 0.93; rabbit: y = 0.33*x-10, slope = 260°/s, R2 = 0.67, cat: y = 0.11*x-4.2, slope = 110°/s, R2 = 0.81. (B) Proportion of saccadic turns on the whole U-turn maneuver. Shown is the average cumulative saccade amplitude (and standard deviation) as a percentage of the whole turn amplitude, with the red line showing the average across birds (n = 72 saccades, N = 5 birds).

Mentions: In contrast to humans, birds shift their gaze mainly through head reorientation (review: [14]). Head saccades can therefore be analyzed to assess gaze performance and strategies. We found that lovebirds performed head saccades more frequently and faster during turning flight. Combined, head saccades made up 76% of the total head reorientation during the turn. Saccade velocities reached values of up to 2700 °/s and are thus, in terms of speed, comparable to head saccades in insects which are three orders of magnitude lighter (Fig 4). Although the head saccade amplitudes are comparable with eye saccade amplitudes of humans and rabbits, lovebirds perform head saccades about three times faster (Fig 5; based on time-resolved tracking data at 2000 Hz). When plotting saccade start position over the flight trajectory, we found that lovebirds make most saccades during the turning phase (Fig 4A, circular markers). Saccades during the turn were typically faster than saccades before or after the turn (see color code in Fig 4A). To compare saccade parameters between birds, we averaged the saccades over individual flights for each bird, before calculating the average across birds. In general, head yaw saccades reached amplitudes up to 60° with a median of 27.7° across birds (Fig 4B). Remarkably, head saccade amplitudes with respect to the arena were comparable to head saccade amplitudes with respect to body yaw orientation (p = 0.96: Friedman test with Bonferroni correction). This shows that head saccade amplitude was not substantially modified by body rotation. Saccade duration varied and had a median at 29.6 ms. The longest recorded saccade lasted 44.5 ms (Fig 4C). While the median head saccade velocity was 926.1°/s across turning birds, rotational head velocities were dramatically reduced during intersaccades to 146.4°/s (Fig 4D). We quantified head yaw velocities relative to the arena and relative to the body (Fig 2C, green line) and averaged them over both the saccadic and intersaccadic phases (Fig 4E). Head yaw velocities with respect to the body were higher between head saccades than absolute yaw velocities with respect to the arena (compare red distributions Fig 4D and 4E; p = 0.03, Friedman test). This shows the extent to which the head was stabilized during intersaccades. In contrast, during head saccades, the head yaw velocity with respect to the body was lower than the yaw velocity with respect to the arena, because the head and body turned in the same direction (compare blue distributions Fig 4D and 4E; p = 0.025, Friedman test). When plotting the distribution of peak saccade velocities with respect to the arena it becomes obvious that most head saccades exceeded velocities over 1000°/s (median 1290°/s). The highest measured head saccade velocity was 2700°/s. This value reaches almost head turning speeds achieved by flying blowflies [27], 1000 times lighter than lovebirds, and it exceeds head turn speeds reported for honey bees [28]. This is even more remarkable considering lovebirds are four times heavier than zebra finches, which they also outperform [3]. The fastest in-flight saccade speed has been reported for fruitflies, performing saccadic body turns which reach 5400°/s during escape maneuvers [29]. Whereas these metrics are impressive, we wondered how saccade amplitude and duration compares across vertebrates.


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

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

Lovebird head rotation is predominantly saccadic at the highest average speed recorded amongst vertebrates.(A) Comparison of horizontal saccade amplitude as a function of its duration. Shown are saccade amplitudes and durations measured in this study (blue triangles, n = 72, N = 5) and data for other species extracted from earlier publications. Gray triangle markers represent the combined eye-head gaze shifts of rhesus macaques (n = 544, N = 2) [30]. Red, green and violet circles illustrate horizontal eye saccades in humans (n = 187, N = 3) [31], rabbits (n = 191, N = 2) [33] and cats (n = 34, N = 2) [32]. We coarsely approximate average head rotation velocities by fitting the data with a linear regression. Line equations: lovebird: y = 1.5*x-14, slope = 1500°/s, R2 = 0.78; rhesus macaque y = 0.4*x+3.4, slope = 400°/s, R2 = 0.69; human: 0.38*x+3.4, slope = 380°/s, R2 = 0.93; rabbit: y = 0.33*x-10, slope = 260°/s, R2 = 0.67, cat: y = 0.11*x-4.2, slope = 110°/s, R2 = 0.81. (B) Proportion of saccadic turns on the whole U-turn maneuver. Shown is the average cumulative saccade amplitude (and standard deviation) as a percentage of the whole turn amplitude, with the red line showing the average across birds (n = 72 saccades, N = 5 birds).
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pone.0129287.g005: Lovebird head rotation is predominantly saccadic at the highest average speed recorded amongst vertebrates.(A) Comparison of horizontal saccade amplitude as a function of its duration. Shown are saccade amplitudes and durations measured in this study (blue triangles, n = 72, N = 5) and data for other species extracted from earlier publications. Gray triangle markers represent the combined eye-head gaze shifts of rhesus macaques (n = 544, N = 2) [30]. Red, green and violet circles illustrate horizontal eye saccades in humans (n = 187, N = 3) [31], rabbits (n = 191, N = 2) [33] and cats (n = 34, N = 2) [32]. We coarsely approximate average head rotation velocities by fitting the data with a linear regression. Line equations: lovebird: y = 1.5*x-14, slope = 1500°/s, R2 = 0.78; rhesus macaque y = 0.4*x+3.4, slope = 400°/s, R2 = 0.69; human: 0.38*x+3.4, slope = 380°/s, R2 = 0.93; rabbit: y = 0.33*x-10, slope = 260°/s, R2 = 0.67, cat: y = 0.11*x-4.2, slope = 110°/s, R2 = 0.81. (B) Proportion of saccadic turns on the whole U-turn maneuver. Shown is the average cumulative saccade amplitude (and standard deviation) as a percentage of the whole turn amplitude, with the red line showing the average across birds (n = 72 saccades, N = 5 birds).
Mentions: In contrast to humans, birds shift their gaze mainly through head reorientation (review: [14]). Head saccades can therefore be analyzed to assess gaze performance and strategies. We found that lovebirds performed head saccades more frequently and faster during turning flight. Combined, head saccades made up 76% of the total head reorientation during the turn. Saccade velocities reached values of up to 2700 °/s and are thus, in terms of speed, comparable to head saccades in insects which are three orders of magnitude lighter (Fig 4). Although the head saccade amplitudes are comparable with eye saccade amplitudes of humans and rabbits, lovebirds perform head saccades about three times faster (Fig 5; based on time-resolved tracking data at 2000 Hz). When plotting saccade start position over the flight trajectory, we found that lovebirds make most saccades during the turning phase (Fig 4A, circular markers). Saccades during the turn were typically faster than saccades before or after the turn (see color code in Fig 4A). To compare saccade parameters between birds, we averaged the saccades over individual flights for each bird, before calculating the average across birds. In general, head yaw saccades reached amplitudes up to 60° with a median of 27.7° across birds (Fig 4B). Remarkably, head saccade amplitudes with respect to the arena were comparable to head saccade amplitudes with respect to body yaw orientation (p = 0.96: Friedman test with Bonferroni correction). This shows that head saccade amplitude was not substantially modified by body rotation. Saccade duration varied and had a median at 29.6 ms. The longest recorded saccade lasted 44.5 ms (Fig 4C). While the median head saccade velocity was 926.1°/s across turning birds, rotational head velocities were dramatically reduced during intersaccades to 146.4°/s (Fig 4D). We quantified head yaw velocities relative to the arena and relative to the body (Fig 2C, green line) and averaged them over both the saccadic and intersaccadic phases (Fig 4E). Head yaw velocities with respect to the body were higher between head saccades than absolute yaw velocities with respect to the arena (compare red distributions Fig 4D and 4E; p = 0.03, Friedman test). This shows the extent to which the head was stabilized during intersaccades. In contrast, during head saccades, the head yaw velocity with respect to the body was lower than the yaw velocity with respect to the arena, because the head and body turned in the same direction (compare blue distributions Fig 4D and 4E; p = 0.025, Friedman test). When plotting the distribution of peak saccade velocities with respect to the arena it becomes obvious that most head saccades exceeded velocities over 1000°/s (median 1290°/s). The highest measured head saccade velocity was 2700°/s. This value reaches almost head turning speeds achieved by flying blowflies [27], 1000 times lighter than lovebirds, and it exceeds head turn speeds reported for honey bees [28]. This is even more remarkable considering lovebirds are four times heavier than zebra finches, which they also outperform [3]. The fastest in-flight saccade speed has been reported for fruitflies, performing saccadic body turns which reach 5400°/s during escape maneuvers [29]. Whereas these metrics are impressive, we wondered how saccade amplitude and duration compares across vertebrates.

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