Doug Altshuler

The ability of birds to change their wing shape allows them to perform complex aerial behaviours. This mechanism, known as wing morphing, affords control over efficiency, stability, and maneuverability during flight. Previous comparative work has shown that dynamic, rather than static, metrics of wing shape are associated with flight behaviour, implying that diverse ecological pressures have caused interspecific variation in wing morphing capacity. However, one aspect of wing morphing has received little attention in the flight biomechanics literature: the propatagium. This region of skin, muscles, and tendons between the shoulder and the wrist has been hypothesized to generate more lift than the skeletal and feather components of the wing, and adjustments to its shape and surface area could affect aerodynamic forces experienced by the bird. Although the propatagium has been informally observed to change shape during wing flexion and extension, its morphing has never been quantified. Here I described how 3D propatagium morphology changes over the wing’s range of motion and across 14 avian species. Propatagium shape was significantly affected by both elbow and wrist angles, but to varying degrees, suggesting an interactive mechanism of skeletal control. Static propatagium shape showed strong phylogenetic signal, but dynamic morphing metrics were not strongly influenced by phylogeny, implying that propatagial morphing, like wing range of motion itself, may instead relate to other factors like flight ecology. Quantification of these metrics provides a basis for further comparative work on dynamic propatagium morphology, as well as investigation of the propatagium’s aerodynamic properties.

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The muscular basis for dynamically changing wing shape in birds is not well understood, owing to the complex and redundant network of muscles in the avian wing as well as a poorly- understood and diverse avian musculature. In passerines the biceps, Tensor Propatagialis Brevis (TPB), and Tensor Propatagialis Longus (TPL) share redundant control of elbow flexion. The TPB and TPL are smaller than the biceps but their lever arms are considerably larger, which suggests that the three muscles should produce similar elbow torque. Another distinct anatomical feature is that the TPL and TPB has have long in-series tendons unlike the biceps. Collectively, the anatomy of theses muscles suggests a hypothesis for the control of elbow flexion in flight: The distally attached TPL and TPB with long in-series tendons act primarily in torque control, whereas the proximally-attached biceps with no in-series tendon acts primarily for position control. To test this hypothesis, I collected EMG and high-speed kinematics on European starlings (Sturnus vulgaris) flying in a wind tunnel under varied conditions. A treatment was applied of attached weights to the distal wing on some flights to alter wing inertia and observe corresponding changes in kinematics and muscle activity suggesting specific muscle control roles. Wing weights did not have a robust effect on elbow kinematics or muscle activity, but EMG, kinematics, and morphology data suggested different functional roles for the three muscles. All three elbow flexors showed peak activity at the beginning of the downstroke, and the biceps demonstrated timing consistent with a role stabilizing the elbow. The TPB and TPL had in vivo timing and morphology consistent with unique roles for wing morphing, with precise and short-duration activity from the TPB consistent with its role in manus extension as well as elbow flexion and a two-pulse response of the TPL consistent with storage and release of elastic energy.

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Birds accomplish an impressive diversity of flight maneuvers primarily through variation in the motion of their wings. It is for this reason that an understanding of wing kinematics is of broad interest to the study of the physics and control of bird flight. However, current optical approaches to animal motion capture struggle to automate the tracking of fixed points on the wing due to the periodic folding and occlusion of flight surfaces during flapping flight. This greatly increases the time and effort needed to record wing kinematics, as the raw data must be digitized by hand. Inthis thesis, I made progress towards a new high-throughput approach to recording wing kinematics using body- and wing-mounted inertial sensors. The data loggers designed for this purpose have a mass of 4g including a battery, and are capable of collecting inertial data from up to four sensors at 450Hz for 20 minutes. An accompanying set of R functions were developed to estimate the orientations of the body and wing segments from the raw inertial data, which in turn were used to estimate joint angles over time. These tools were validated against an optical motion capturesystem and were able estimate the orientation of individual bodies within 3° and angles between bodies within 6° in controlled tests. However, the tools could not be used to record the wing kinematics of pigeons because the angular velocity of the wings exceeded the sensing range of the gyroscopes used in the current design. Specialized high-range gyroscopes are commercially available and could be incorporated into future designs to overcome this limitation. Inertial motion capture has the potential to be a high-throughput, cost-effective, and portable alternative to high-speed video for recording wing kinematics in freely flying birds. This approach could also be used to record detailed kinematics in other animal systems where optical motion capture is infeasible, such as in situations with poor visibility or to study behaviours that occur over large spatial scales.

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Global visual motion across the retina due to self-motion is called optic flow. Optic flow is an important idiothetic cue for locomotion control. In birds, the lentiformis mesencephali (LM) and the nucleus of the basal optic root (nBOR) of the midbrain process optic flow and transmit it to the cerebellum for integration with other sensory inputs. The vestibulocerebellum (VbC), composed of folium IXcd and X, is important for visuomotor control and has been divided into several functional sagittal compartments, defined by multiple factors. Purkinje cells in the VbC differentially express a molecular marker, zebrin II, generating parasagittal zebrin immuno-positive bands alternating with zebrin immuno-negative bands. Both the LM and the nBOR project directly to the VbC as mossy fibers and are co-localized within immuno-positive bands. The LM and nBOR also project indirectly to the VbC via the medial column of the inferior olive (mcIO). The mcIO cells project as climbing fibers to the VbC. In pigeons, the LM projects to the caudal mcIO and the nBOR project to the rostral mcIO. These pathways have not been explored to the same detail in other avian species. I dual-injected anterograde tracers of different fluorescence in the LM and the nBOR of zebra finches and traced the projections to the mcIO and VbC. Folium IXcd was also immunolabeled for zebrin II. I show that the zebra finch inferior olive has a more complex structure than previously reported in other birds. The nBOR axon terminals can be found in most of the mcIO subdivisions, whereas the LM terminals are mostly in the dorsal divisions. The zebrin expression and the mossy fiber distribution patterns are in general similar between zebra finches and pigeons. However, further analysis revealed that LM has more projections to per unit area of the immuno-positive bands, whereas more nBOR mossy fiber terminals were found in the area-corrected immuno-negative bands. The present study suggests that species differences in visuomotor pathways exist and zebra finches may serve as an important species to understand the evolution of the neuroanatomy that supports birds to perform different flight behaviors.

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A major visual signal for control of posture and movement is optic flow - the global motion across the retina due to relative motion between an organism and its environment. In birds, the pretectum and accessory optic system of the midbrain consist of neurons that are sensitive to optic flow. The retinal recipient nuclei for these key pathways are the lentiformis mesencephali (LM) and the nucleus of the basal optic root (nBOR). Over a decade, research from pigeons (Columba livia) revealed that both retinal recipient optic flow nuclei send projections to the cerebellum. The vestibulocerebellum (folium IX) receives strong input from both LM and nBOR. The oculomotor cerebellum (folia VI-VIII) also received LM input. Recently, the inputs to the vestibulocerebellum and the oculomotor cerebellum were measured in two additional species, Anna's hummingbirds (Calypte anna) and zebra finches (Taeniopygia guttata). The midbrain-cerebellar pathways differed among species in several unexpected ways. The hummingbird oculomotor cerebellum received half of it inputs from the LM and half from two other midbrain areas, the nucleus laminaris precommisuralis (LPC) and the nucleus principalis precommisuralis (PPC). In the zebra finch, the oculomotor cerebellum received 75% of its inputs from LPC and PPC. Thus, the recent work suggests important roles for LPC and PPC in oculomotor control. This result is surprising because in the pigeon, these two nuclei represent only 7.9% of the inputs to the oculomotor cerebellum. Relatively little is known about either LPC or PPC.The goal of my thesis was to answer two questions about these circuits: 1) Do LPC and PPC neurons of zebra finches and hummingbirds that project to oculomotor cerebellum also receive retinal inputs? 2) Do retinal ganglion cells of hummingbirds and zebra finches project to other brain regions not currently described for birds? Both questions were addressed by injecting Cholera Toxin B with different fluorophores into the oculomotor cerebellum and the eye. These experiments revealed a novel one-synapse pathway from the eye to the cerebellum in LPC, but not in PPC. I also confirmed a second one-synapse pathway through the area pretectalis that had been proposed from earlier single injection studies.

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A moving animal experiences global visual signals across the entire retina known as optic flow, one of the key signals used in the visual guidance of locomotion. Optic flow sensitive neurons have been identified in the midbrains of all vertebrate classes. In birds, these neurons are found in the nucleus of the basal optic root (nBOR) and the pretectal nucleus lentiformis mesencephali (LM). These cells are known to exhibit large receptive fields in the contralateral eye, are excited by visual motion in a “preferred” direction and are inhibited by motion in the opposite direction. A key question is whether the response properties of LM neurons are conserved across species or are LM neurons specialized in animals that use different locomotor strategies. Previous studies in pigeons have investigated the responses of neurons in the LM and nBOR to drifting sine-wave gratings and discovered that they are tuned in the spatiotemporal domain. The LM typically contains cells that respond maximally to fast stimuli and are tuned to temporal frequency whereas nBOR cells respond maximally to slower stimuli and are velocity-tuned. Here we ask whether zebra finches and hummingbirds, specialized for different modes of locomotion, exhibit spatiotemporal specializations in optic flow neurons that may be related to their form of locomotion. We explored this question by making extracellular recordings in the LM of anesthetized birds while presenting drifting sine-wave gratings to the contralateral eye. These results were compared with previous pigeon data and we found that each of the three species exhibits distinct tuning in the spatiotemporal domain. Hummingbird LM neurons are tuned to the fastest stimuli, which were typically of lower spatial frequencies. Both hummingbird and finch LM cells exist almost exclusively as fast cells with 90% of peaks in the fast zone. Moreover, in pigeons, only ‘slow’ cells are velocity tuned, whereas both zebra finches and hummingbirds have ‘fast’ cells that are velocity tuned. These species-specific differences are suggestive of neural specializations for different optic flow behavior.

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Birds flying in turbulent conditions demonstrate impressive flight stability and control. This versatility is hypothesized to derive from dynamic wing shape changes, an ability termed wing morphing. Bird wings can morph passively through inertial or aerodynamic loading of flexible components or actively when birds stimulate their network of intrinsic wing muscles. The majority of active wing morphing is actuated through the wrist or elbow joints. Wrist flexion improves high-speed and turning performance, but little is known about the morphology or aerodynamic consequences of morphing the elbow joint. Here we show that gulls gliding in unsteady environments reduce their passive stability by actively reducing their elbow angle. We first photographed gulls in gliding flight to quantify their wing shapes. We next used cadavers to determine the viable range of elbow angles and isolate the subset that was used by gliding gulls. The behavioral observations and cadaver manipulations revealed an in vivo gliding elbow angle range of 90°-154° and that there is a significant reduction of the elbow angle used by gulls as local wind speeds and gusts increase. Next, wings were prepared and dried across the full range of elbow angles and tested in a wind tunnel at varied turbulence intensities. These force measurements revealed that the lower elbow angles used by gliding gulls had improved aerodynamic efficiency but reduced passive pitch stability. Moreover, we found that the in vivo elbow range captures the majority of the available aerodynamic variation. Collectively, our results indicate a coupling in efficiency and stability in avian gliding and that wing morphing allows gulls to modulate aerodynamic trade-offs which may allow for a steadier flight path in an unsteady environment.

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Avian wings change shape during the flapping cycle due to the activity of a network of intrinsic wing muscles. Wing control is believed to be the key feature allowing birds to maneuver safely through different environments. One control aspect is elbow joint motion, which relates to wing folding for the upstroke and re-expansion for the downstroke. Muscle anatomy suggests that if the muscles are actuating then the biceps flex the elbow, and the two heads of the triceps, the humerotriceps and scapulotriceps, extend the elbow. This set of antagonist muscles could thus actively modulate wing shape by regulating elbow joint angle. Control of the elbow joint angle remains uncertain as motor elements can have diverse functions such as actuators, brakes, springs, and struts, where specific roles and their magnitudes depend on when muscles are activated in the contractile cycle. The wing muscles best studied during flight are the elbow muscles of the pigeon (Columba livia). In vivo studies during different flight modes revealed variation in strain profile, activation timing and duration, and in contractile cycle frequency of the humerotriceps. This variation suggests that the pigeon humerotriceps may alter wing shape in diverse ways. To test this hypothesis, I developed an in situ work loop technique to measure the performance of the pigeon humerotriceps. My experiments tested how activation duration and contractile cycle frequency influenced muscle work and power across the full range of activation onset times. I found that the humerotriceps generated net positive power over a narrow range of activation times. The humerotriceps produced predominantly net negative power, likely due to relatively long activation durations, indicating that it absorbs work, but the work loop shapes also suggest varying degrees of elasticity and resistance. I was unable to examine the effects of variation in strain profile because current work loop technology does not allow for this. Nonetheless, these results, when combined with previous in vivo studies, show that the humerotriceps can dynamically shift among roles of brake, spring, and strut, based on activation properties that vary with flight mode.

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Flying animals are hypothesized to direct the lateral force necessary to execute turns through two methods. The first is force vectoring, which is accomplished by banking the wing stroke plane and body in concert. Through this method, centripetal force is provided by the lateral component of aerodynamic force that is directed into a turn. An alternative hypothesis is that they generate lateral force through asymmetries in wingbeat kinematics between the left and right wings without varying body position. Examples of asymmetrical kinematics could include differences in angle of attack, stroke plane angle, or stroke amplitude. We studied turning hummingbirds as they tracked a revolving feeder to distinguish between these mechanisms. Comparing hovering and turning flight revealed that hummingbirds bank their stroke plane and body into turns and maintain the position of the stroke plane relative to their bodies, supporting a force vectoring mechanism. However, several wingbeat asymmetries were observed during turning, such as the outer wing tip path being higher and flatter, and the inner wing tip path being lower and more scooped than in hovering. Because the centripetal force necessary to complete a turn is determined by translational velocity and turn radius, we created four balanced turning treatments where these aspects of a turn were varied with a revolving feeder to determine how wing and body kinematics change in order to compensate for these challenges. We found that three asymmetric wingbeat kinematic variables were associated with changes in turn radius and two body kinematic variables related to force vectoring were associated with changes in translational velocity. There were no kinematics influenced by both radius and velocity. This suggests wingbeat asymmetries compensate for changes in turning radius and force vectoring is used to compensate for changes in velocity. Thus, rather than force vectoring and wingbeat asymmetries being mutually exclusive, our results indicate that the two mechanisms are used simultaneously and independently to meet different aerodynamic challenges.

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The sampling of spatial and temporal visual information for all living organisms is finite. The speed and accuracy of visual systems contributes in part to an animal's sensitivity to visual motion. The ability to see swift motions is a crucial adaptation among bird species, which are high-speed animals that navigate in a three-dimensional world. Hummingbirds are emerging as important models for studying visual guidance in vertebrates. However, their sensitivity to visual motion remains unknown. A method that can be used to identify hummingbirds' sensitivity to visual motion is to characterise the spatial and temporal acuity of their visual system. It is hypothesised that temporal acuity scales positively with mass-specific metabolic rate and negatively with body size, and spatial acuity scales positively with body size. Given hummingbirds possess the highest mass- specific metabolic rates among vertebrates and the smallest body sizes among birds, I predicted that the Anna's hummingbird (Calypte anna) would have high temporal and low spatial acuities among bird species. Using operant conditioning and optocollic reflex experiments, I identified the temporal and spatial acuity thresholds of the Anna's hummingbird's visual system. Training hummingbirds to differentiate flickering from non-flickering lights at different rates and colours measured their temporal acuity for wavelengths of light between 380-750nm. Spatial acuity was measured by subjecting hummingbirds to rotating stimuli that varied in spatial frequency and luminance. The results indicate the hummingbird's temporal acuity is between 70 and 80Hz, and is unaffected by light colour (red, white, and ultraviolet). Spatial resolving capacity is measured to be between 4.95 and 6.18 cycles per degree in light conditions below 1.77 candela/m². Therefore, my measurements of spatial acuity in the Anna's hummingbird provide support for a positive relationship with body size, and my measurements of temporal acuity do not provide support for a positive relationship with mass-specific metabolic rate. This study marks the first time both spatial and temporal acuity is measured in a sustained hovering animal.

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This thesis presents a new three-dimensional atlas for analyzing the neuroanatomical structures of the avian brain. Using magnetic resonance imaging (MRI) and X-ray computed tomography (CT), the brain of an Anna’s Hummingbird (Calypte anna) was scanned. These datasets were co-registered using three-dimensional visualisation software and overlaid with thionin stained slices in the sagittal and coronal view. Results show that previously developed techniques for creating three-dimensional atlases in other birds can be successfully used for representing the anatomical structures of hummingbirds (Güntürkün et al., 2013; Poirier et al., 2008; Vellema et al., 2011). There is no previous atlas, neither two nor three-dimensional, available for hummingbirds or any other wild-caught bird. Studies requiring avian neural recordings have not included hummingbirds, but this combination of imaging protocols along with descriptions from the literature provides the necessary and sufficient information for outlining many of the major functional structures in the Anna’s hummingbird brain. The co-registered datasets are also sufficient for constructing histological data into a three-dimensional representation that is functional in guiding classical tract tracing and electrophysiology experiments. By creating brain area delineations in three dimensions and anchoring these data to a skull, researchers will now be able to reach target structures from outside of the brain. For two regions of the brain, the lentiformis mesencephali and nucleus of the basal optic route, suggested stereotaxic coordinates and angles are provided. Through expanding the collection of atlases to include hummingbirds we introduce a new animal that will be especially useful for future studies of avian motor control.

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