Limits...
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 improve visual flight control by coordinating super-fast gaze shifts with the end of their downstroke.(A) Top view schematic of a typical recording that shows that the wings occlude the lateral visual field at the end of the downstroke. The lovebird’s azimuthal visual field is approximated from ophthalmologic measurements at the visual equator of Senegal parrots [57]. (B) For demonstrative purposes a lovebird was filmed from the side during a turning on a dime maneuver with the side panels of the arena removed (this video sequence is not part of the data analysis). (C) Most saccades were initiated at 75% of the downstroke (see Fig 3B), when the wings occlude more than half of the lateral visual field.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4481315&req=5

pone.0129287.g008: Lovebirds improve visual flight control by coordinating super-fast gaze shifts with the end of their downstroke.(A) Top view schematic of a typical recording that shows that the wings occlude the lateral visual field at the end of the downstroke. The lovebird’s azimuthal visual field is approximated from ophthalmologic measurements at the visual equator of Senegal parrots [57]. (B) For demonstrative purposes a lovebird was filmed from the side during a turning on a dime maneuver with the side panels of the arena removed (this video sequence is not part of the data analysis). (C) Most saccades were initiated at 75% of the downstroke (see Fig 3B), when the wings occlude more than half of the lateral visual field.

Mentions: Lovebirds performing a rapid ‘turn on a dime’ maneuver shift their gaze between arena features with superfast head saccades. These gaze shifts reach on average 930°/s with peaks up to 2690°/s, the fastest recorded saccades for vertebrates to date [14,36] (Fig 5A). This speed compares to the saccade speeds reported for flying insects that are up to three orders of magnitudes lighter than lovebirds [27] (Fig 4F). These extraordinarily fast turns are made possible by the highly specialized avian neck system, of which the muscles contract effectively as fast as the flight muscles [43]. Between saccades, lovebirds stabilize their head towards prominent arena features in the frontal visual field (Fig 6). Compared to the head, body rotations are continuous and slower, lacking the characteristics of saccades (Fig 2C, S1 Movie). This finding indicates that flying lovebirds perform a gaze strategy that facilitates optic flow processing [3,44,45]: They are separating distance dependent translational optic flow from distant independent rotational optic flow cues at the behavioral level. This optic flow orchestration simplifies neural processing [8,45] in visual brain centers [46–50], which facilitates the extraction of relative proximity and heading information. A similar head turn behavior has been reported for turning pigeons [51]. However, due to the different focus of their study, Bilo and colleagues interpreted their findings mainly within the framework of reflexive neck and wing control mechanisms [51]. Our finding that lovebirds landing on a moving perch experience low variation in retinal perch size, supports the hypothesis that landing birds use this cue for visual flight control, in addition to self-motion related parameters [5]. Lovebirds shift their gaze between arena features using super-fast saccades that are timed with the last quarter of the wings’ downstroke (Fig 3B). As their wings occlude lateral vision during this stroke phase, lovebirds maximize visual perception by overlying behaviors that impair vision (Fig 8). In flying bats a similar coupling between wing kinematics and acoustic sensing was found. Their respiration and ultrasonic calls are related to their wingbeat frequency [52–54]. By analyzing the wingbeat frequency of maneuvering lovebirds, we find them to be intermittent as reported for other small generalist birds [55,56]. Interestingly, lovebirds compose their wingbeat of two distinct flapping modes (Fig 3A). During their slower flapping mode of 9.5 Hz, upstrokes are twice as long as downstrokes while downstrokes are slightly longer in the normal flapping mode of 17 Hz. When turning, lovebirds perform preferably normal wingbeats and, accordingly, most observed saccadic gaze shift are coordinated within this flapping mode.


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

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

Lovebirds improve visual flight control by coordinating super-fast gaze shifts with the end of their downstroke.(A) Top view schematic of a typical recording that shows that the wings occlude the lateral visual field at the end of the downstroke. The lovebird’s azimuthal visual field is approximated from ophthalmologic measurements at the visual equator of Senegal parrots [57]. (B) For demonstrative purposes a lovebird was filmed from the side during a turning on a dime maneuver with the side panels of the arena removed (this video sequence is not part of the data analysis). (C) Most saccades were initiated at 75% of the downstroke (see Fig 3B), when the wings occlude more than half of the lateral visual field.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4481315&req=5

pone.0129287.g008: Lovebirds improve visual flight control by coordinating super-fast gaze shifts with the end of their downstroke.(A) Top view schematic of a typical recording that shows that the wings occlude the lateral visual field at the end of the downstroke. The lovebird’s azimuthal visual field is approximated from ophthalmologic measurements at the visual equator of Senegal parrots [57]. (B) For demonstrative purposes a lovebird was filmed from the side during a turning on a dime maneuver with the side panels of the arena removed (this video sequence is not part of the data analysis). (C) Most saccades were initiated at 75% of the downstroke (see Fig 3B), when the wings occlude more than half of the lateral visual field.
Mentions: Lovebirds performing a rapid ‘turn on a dime’ maneuver shift their gaze between arena features with superfast head saccades. These gaze shifts reach on average 930°/s with peaks up to 2690°/s, the fastest recorded saccades for vertebrates to date [14,36] (Fig 5A). This speed compares to the saccade speeds reported for flying insects that are up to three orders of magnitudes lighter than lovebirds [27] (Fig 4F). These extraordinarily fast turns are made possible by the highly specialized avian neck system, of which the muscles contract effectively as fast as the flight muscles [43]. Between saccades, lovebirds stabilize their head towards prominent arena features in the frontal visual field (Fig 6). Compared to the head, body rotations are continuous and slower, lacking the characteristics of saccades (Fig 2C, S1 Movie). This finding indicates that flying lovebirds perform a gaze strategy that facilitates optic flow processing [3,44,45]: They are separating distance dependent translational optic flow from distant independent rotational optic flow cues at the behavioral level. This optic flow orchestration simplifies neural processing [8,45] in visual brain centers [46–50], which facilitates the extraction of relative proximity and heading information. A similar head turn behavior has been reported for turning pigeons [51]. However, due to the different focus of their study, Bilo and colleagues interpreted their findings mainly within the framework of reflexive neck and wing control mechanisms [51]. Our finding that lovebirds landing on a moving perch experience low variation in retinal perch size, supports the hypothesis that landing birds use this cue for visual flight control, in addition to self-motion related parameters [5]. Lovebirds shift their gaze between arena features using super-fast saccades that are timed with the last quarter of the wings’ downstroke (Fig 3B). As their wings occlude lateral vision during this stroke phase, lovebirds maximize visual perception by overlying behaviors that impair vision (Fig 8). In flying bats a similar coupling between wing kinematics and acoustic sensing was found. Their respiration and ultrasonic calls are related to their wingbeat frequency [52–54]. By analyzing the wingbeat frequency of maneuvering lovebirds, we find them to be intermittent as reported for other small generalist birds [55,56]. Interestingly, lovebirds compose their wingbeat of two distinct flapping modes (Fig 3A). During their slower flapping mode of 9.5 Hz, upstrokes are twice as long as downstrokes while downstrokes are slightly longer in the normal flapping mode of 17 Hz. When turning, lovebirds perform preferably normal wingbeats and, accordingly, most observed saccadic gaze shift are coordinated within this flapping mode.

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