The spatiotemporal richness of hummingbird wing deformations.

Animals exhibit an abundant diversity of forms, and this diversity is even more evident when considering animals that can change shape on demand. The evolution of flexibility contributes to aspects of performance from propulsive efficiency to environmental navigation. It is, however, challenging to quantify and compare body parts that, by their nature, dynamically vary in shape over many time scales. Commonly, body configurations are tracked by labelled markers and quantified parametrically through conventional measures of size and shape (descriptor approach) or non-parametrically through data-driven analyses that broadly capture spatiotemporal deformation patterns (shape variable approach). We developed a weightless marker tracking technique and combined these analytic approaches to study wing morphological flexibility in hoverfeeding Anna's hummingbirds (Calypte anna). Four shape variables explained >95% of typical stroke cycle wing shape variation and were broadly correlated with specific conventional descriptors such as wing twist and area. Moreover, shape variables decomposed wing deformations into pairs of in-plane and out-of-plane components at integer multiples of the stroke frequency. This property allowed us to identify spatiotemporal deformation profiles characteristic of hoverfeeding with experimentally imposed kinematic constraints, including through shape variables explaining <10% of typical shape variation. Hoverfeeding in front of a visual barrier restricted stroke amplitude and elicited increased stroke frequencies together with in-plane and out-of-plane deformations throughout the stroke cycle. Lifting submaximal loads increased stroke amplitudes at similar stroke frequencies together with prominent in-plane deformations during the upstroke and pronation. Our study highlights how spatially and temporally distinct changes in wing shape can contribute to agile fluidic locomotion.

Hummingbirds use distinct control strategies for forward and hovering flight.

The detection of optic flow is important for generating optomotor responses to mediate retinal image stabilization, and it can also be used during ongoing locomotion for centring and velocity control. Previous work in hummingbirds has separately examined the roles of optic flow during hovering and when centring through a narrow passage during forward flight. To develop a hypothesis for the visual control of forward flight velocity, we examined the behaviour of hummingbirds in a flight tunnel where optic flow could be systematically manipulated. In all treatments, the animals exhibited periods of forward flight interspersed with bouts of spontaneous hovering. Hummingbirds flew fastest when they had a reliable signal of optic flow. All optic flow manipulations caused slower flight, suggesting that hummingbirds had an expected optic flow magnitude that was disrupted. In addition, upward and downward optic flow drove optomotor responses for maintaining altitude during forward flight. When hummingbirds made voluntary transitions to hovering, optomotor responses were observed to all directions. Collectively, these results are consistent with hummingbirds controlling flight speed via mechanisms that use an internal forward model to predict expected optic flow whereas flight altitude and hovering position are controlled more directly by sensory feedback from the environment.

Topography of visual and somatosensory inputs to the pontine nuclei in zebra finches (Taeniopygia guttata).

Birds have a comprehensive network of sensorimotor projections extending from the forebrain and midbrain to the cerebellum via the pontine nuclei, but the organization of these circuits in the pons is not thoroughly described. Inputs to the pontine nuclei include two retinorecipient areas, nucleus lentiformis mesencephali (LM) and nucleus of the basal optic root (nBOR), which are important structures for analyzing optic flow. Other crucial regions for visuomotor control include the retinorecipient ventral lateral geniculate nucleus (GLv), and optic tectum (TeO). These visual areas, together with the somatosensory area of the anterior (rostral) Wulst, which is homologous to the primary somatosensory cortex in mammals, project to the medial and lateral pontine nuclei (PM, PL). In this study, we used injections of fluorescent tracers to study the organization of these visual and somatosensory inputs to the pontine nuclei in zebra finches. We found a topographic organization of inputs to PM and PL. The PM has a lateral subdivision that predominantly receives projections from the ipsilateral anterior Wulst. The medial PM receives bands of inputs from the ipsilateral GLv and the nucleus laminaris precommisulis, located medial to LM. We also found that the lateral PL receives a strong ipsilateral projection from TeO, while the medial PL and region between the PM and PL receive less prominent projections from nBOR, bilaterally. We discuss these results in the context of the organization of pontine inputs to the cerebellum and possible functional implications of diverse somato-motor and visuomotor inputs and parcellation in the pontine nuclei.

From the eye to the wing: neural circuits for transforming optic flow into motor output in avian flight.

Avian flight is guided by optic flow-the movement across the retina of images of surfaces and edges in the environment due to self-motion. In all vertebrates, there is a short pathway for optic flow information to reach pre-motor areas: retinal-recipient regions in the midbrain encode optic flow, which is then sent to the cerebellum. One well-known role for optic flow pathways to the cerebellum is the control of stabilizing eye movements (the optokinetic response). However, the role of this pathway in controlling locomotion is less well understood. Electrophysiological and tract tracing studies are revealing the functional connectivity of a more elaborate circuit through the avian cerebellum, which integrates optic flow with other sensory signals. Here we review the research supporting this framework and identify the cerebellar output centres, the lateral (CbL) and medial (CbM) cerebellar nuclei, as two key nodes with potentially distinct roles in flight control. The CbM receives bilateral optic flow information and projects to sites in the brainstem that suggest a primary role for flight control over time, such as during forward flight. The CbL receives monocular optic flow and other types of visual information. This site provides feedback to sensory areas throughout the brain and has a strong projection the nucleus ruber, which is known to have a dominant role in forelimb muscle control. This arrangement suggests primary roles for the CbL in the control of wing morphing and for rapid maneuvers.

Topography of optic flow processing in olivo-cerebellar pathways in zebra finches (Taeniopygia guttata).

In birds, the nucleus of the basal optic root (nBOR) and the nucleus lentiformis mesencephali (LM) are brainstem nuclei involved in the analysis of optic flow. A major projection site of both nBOR and LM is the medial column of the inferior olive (IO), which provides climbing fibers to the vestibulocerebellum. This pathway has been well documented in pigeons, but not other birds. Recent works have highlighted that zebra finches show specializations with respect to optic flow processing, which may be reflected in the organization of optic flow pathways to the IO. In this study, we characterized the organization of these pathways in zebra finches. We found that the medial column consists of at least eight subnuclei (i-viii) visible in Nissl-stained tissue. Using anterograde traces we found that the projections from LM and nBOR to the IO were bilateral, but heavier to the ipsilateral side, and showed a complementary pattern: LM projected to subnucleus i, whereas nBOR projected to subnuclei ii and v. Using retrograde tracers, we found that these subnuclei (i, ii and v) projected to the vestibulocerebellum (folia IXcd and X), whereas the other subnuclei projected to IXab and the lateral margin of VII and VIII. The nBOR also projected ipsilaterally to the caudo-medial dorsal lamella of the IO, which the retrograde experiments showed as projecting to the medial margin of VII and VIII. We compare these results with previous studies in other avian species.

Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds.

Hummingbirds possess distinct metabolic adaptations to fuel their energy-demanding hovering flight, but the underlying genomic changes are largely unknown. Here, we generated a chromosome-level genome assembly of the long-tailed hermit and screened for genes that have been specifically inactivated in the ancestral hummingbird lineage. We discovered that FBP2 (fructose-bisphosphatase 2), which encodes a gluconeogenic muscle enzyme, was lost during a time period when hovering flight evolved. We show that FBP2 knockdown in an avian muscle cell line up-regulates glycolysis and enhances mitochondrial respiration, coincident with an increased mitochondria number. Furthermore, genes involved in mitochondrial respiration and organization have up-regulated expression in hummingbird flight muscle. Together, these results suggest that FBP2 loss was likely a key step in the evolution of metabolic muscle adaptations required for true hovering flight.

Specializations in optic flow encoding in the pretectum of hummingbirds and zebra finches.

All visual animals experience optic flow-global visual motion across the retina, which is used to control posture and movement.1 The midbrain circuitry for optic flow is highly conserved in vertebrates,2-6 and these neurons show similar response properties across tetrapods.4,7-16 These neurons have large receptive fields and exhibit both direction and velocity selectivity in response to large moving stimuli. Hummingbirds deviate from the typical vertebrate pattern in several respects.17,18 Their lentiformis mesencephali (LM) lacks the directional bias seen in other tetrapods and has an overall bias for faster velocities. This led Ibbotson19 to suggest that the hummingbird LM may be specialized for hovering close to visual structures, such as plants. In such an environment, even slight body motions will translate into high-velocity optic flow. A prediction from this hypothesis is that hummingbird LM neurons should be more responsive to large visual features. We tested this hypothesis by measuring neural responses of hummingbirds and zebra finches to sine wave gratings of varying spatial and temporal frequencies. As predicted, the hummingbird LM displayed an overall preference for fast optic flow because neurons were biased to lower spatial frequencies. These neurons were also tightly tuned in the spatiotemporal domain. We found that the zebra finch LM specializes along another domain: many neurons were initially tuned to high temporal frequencies followed by a shift in location and orientation to slower velocity tuning. Collectively, these results demonstrate that the LM has distinct and specialized tuning properties in at least two bird species.

Response properties of optic flow neurons in the accessory optic system of hummingbirds versus zebra finches and pigeons.

Optokinetic responses function to maintain retinal image stabilization by minimizing optic flow that occurs during self-motion. The hovering ability of hummingbirds is an extreme example of this behavior. Optokinetic responses are mediated by direction-selective neurons with large receptive fields in the accessory optic system (AOS) and pretectum. Recent studies in hummingbirds showed that, compared with other bird species, 1) the pretectal nucleus lentiformis mesencephali (LM) is hypertrophied, 2) LM has a unique distribution of direction preferences, and 3) LM neurons are more tightly tuned to stimulus velocity. In this study, we sought to determine if there are concomitant changes in the nucleus of the basal optic root (nBOR) of the AOS. We recorded the visual response properties of nBOR neurons to large-field-drifting random dot patterns and sine-wave gratings in Anna's hummingbirds and zebra finches and compared these with archival data from pigeons. We found no differences with respect to the distribution of direction preferences: Neurons responsive to upward, downward, and nasal-to-temporal motion were equally represented in all three species, and neurons responsive to temporal-to-nasal motion were rare or absent (<5%). Compared with zebra finches and pigeons, however, hummingbird nBOR neurons were more tightly tuned to stimulus velocity of random dot stimuli. Moreover, in response to drifting gratings, hummingbird nBOR neurons are more tightly tuned in the spatiotemporal domain. These results, in combination with specialization in LM, support a hypothesis that hummingbirds have evolved to be "optic flow specialists" to cope with the optomotor demands of sustained hovering flight.NEW & NOTEWORTHY Hummingbirds have specialized response properties to optic flow in the pretectal nucleus lentiformis mesencephali (LM). The LM works with the nucleus of the basal optic root (nBOR) of the accessory optic system (AOS) to process global visual motion, but whether the neural response specializations observed in the LM extend to the nBOR is unknown. Hummingbird nBOR neurons are more tightly tuned to visual stimulus velocity, and in the spatiotemporal domain, compared with two nonhovering species.

Phase transformation-driven artificial muscle mimics the multifunctionality of avian wing muscle.

Skeletal muscle provides a compact solution for performing multiple tasks under diverse operational conditions, a capability lacking in many current engineered systems. Here, we evaluate if shape memory alloy (SMA) components can serve as artificial muscles with tunable mechanical performance. We experimentally impose cyclic stimuli, electric and mechanical, to an SMA wire and demonstrate that this material can mimic the response of the avian humerotriceps, a skeletal muscle that acts in the dynamic control of wing shapes. We next numerically evaluate the feasibility of using SMA springs as artificial leg muscles for a bipedal walking robot. Altering the phase offset between mechanical and electrical stimuli was sufficient for both synthetic and natural muscle to shift between actuation, braking and spring-like behaviour.

Flight muscle power increases with strain amplitude and decreases with cycle frequency in zebra finches (Taeniopygia guttata).

Birds that use high flapping frequencies can modulate aerodynamic force by varying wing velocity, which is primarily a function of stroke amplitude and wingbeat frequency. Previous measurements from zebra finches (Taeniopygia guttata) flying across a range of speeds in a wind tunnel demonstrate that although the birds modulated both wingbeat kinematic parameters, they exhibited greater changes in stroke amplitude. These two kinematic parameters contribute equally to aerodynamic force, so the preference for modulating amplitude over frequency may instead derive from limitations of muscle physiology at high frequency. We tested this hypothesis by developing a novel in situ work loop approach to measure muscle force and power output from the whole pectoralis major of zebra finches. This method allowed for multiple measurements over several hours without significant degradation in muscle power. We explored the parameter space of stimulus, strain amplitude and cycle frequencies measured previously from zebra finches, which revealed overall high net power output of the muscle, despite substantial levels of counter-productive power during muscle lengthening. We directly compared how changes to muscle shortening velocity via strain amplitude and cycle frequency affected muscle power. Increases in strain amplitude led to increased power output during shortening with little to no change in power output during lengthening. In contrast, increases in cycle frequency did not lead to increased power during shortening but instead increased counter-productive power during lengthening. These results demonstrate why at high wingbeat frequency, increasing wing stroke amplitude could be a more effective mechanism to cope with increased aerodynamic demands.

An Algorithmic Approach to Natural Behavior.

Uncovering the mechanisms and implications of natural behavior is a goal that unites many fields of biology. Yet, the diversity, flexibility, and multi-scale nature of these behaviors often make understanding elusive. Here, we review studies of animal pursuit and evasion - two special classes of behavior where theory-driven experiments and new modeling techniques are beginning to uncover the general control principles underlying natural behavior. A key finding of these studies is that intricate sequences of pursuit and evasion behavior can often be constructed through simple, repeatable rules that link sensory input to motor output: we refer to these rules as behavioral algorithms. Identifying and mathematically characterizing these algorithms has led to important insights, including the discovery of guidance rules that attacking predators use to intercept mobile prey, and coordinated neural and biomechanical mechanisms that animals use to avoid impending collisions. Here, we argue that algorithms provide a good starting point for studies of natural behavior more generally. Rather than beginning at the neural or ecological levels of organization, we advocate starting in the middle, where the algorithms that link sensory input to behavioral output can provide a solid foundation from which to explore both the implementation and the ecological outcomes of behavior. We review insights that have been gained through such an algorithmic approach to pursuit and evasion behaviors. From these, we synthesize theoretical principles and lay out key modeling tools needed to apply an algorithmic approach to the study of other complex natural behaviors.

Hummingbird vision.

Hummingbirds are widely recognized by their hovering flight. In this Quick guide, Altshuler and Wylie describe the visual specializations that allow for the hummingbird's flight abilities.

Spatial and Temporal Resolution of the Visual System of the Anna's Hummingbird (Calypte anna) Relative to Other Birds.

Hummingbirds are an emerging model for studies of the visual guidance of flight. However, basic properties of their visual systems, such as spatial and temporal visual resolution, have not been characterized. We measured both the spatial and temporal visual resolution of Anna's hummingbirds using behavioral experiments and anatomical estimates. Spatial visual resolution was determined behaviorally using the optocollic reflex and anatomically using peak retinal ganglion cell densities from retinal whole mounts and eye size. Anna's hummingbirds have a spatial visual resolution of 5-6 cycles per degree when measured behaviorally, which matches anatomical estimates (fovea: 6.26±0.12 cycles per degree; area temporalis: 5.59±0.15 cycles per degree; and whole eye average: 4.64±0.08 ). To determine temporal visual resolution, we used an operant conditioning paradigm wherein hummingbirds were trained to use a flickering light to find a food reward. The limits of temporal visual resolution were estimated as 70-80 Hz. To compare Anna's hummingbirds with other bird species, we used a phylogenetically controlled analysis of previously published data on avian visual resolutions and body size. Our measurements for Anna's hummingbird vision fall close to and below predictions based on body size for spatial visual resolution and temporal visual resolution, respectively. These results indicate that the enhanced flight performance and foraging behaviors of hummingbirds do not require enhanced spatial or temporal visual resolution. This finding is important for interpreting flight control studies and contributes to a growing understanding of avian vision.

Pretectal projections to the oculomotor cerebellum in hummingbirds (Calypte anna), zebra finches (Taeniopygia guttata), and pigeons (Columba livia).

In birds, optic flow is processed by a retinal-recipient nucleus in the pretectum, the nucleus lentiformis mesencephali (LM), which then projects to the cerebellum, a key site for sensorimotor integration. Previous studies have shown that the LM is hypertrophied in hummingbirds, and that LM cell response properties differ between hummingbirds and other birds. Given these differences in anatomy and physiology, we ask here if there are also species differences in the connectivity of the LM. The LM is separated into lateral and medial subdivisions, which project to the oculomotor cerebellum and the vestibulocerebellum. In pigeons, the projection to the vestibulocerebellum largely arises from the lateral LM; the projection to the oculomotor cerebellum largely arises from the medial LM. Here, using retrograde tracing, we demonstrate differences in the distribution of projections in these pathways between Anna's hummingbirds (Calypte anna), zebra finches (Taeniopygia guttata), and pigeons (Columba livia). In all three species, the projections to the vestibulocerebellum were largely from lateral LM. In contrast, projections to the oculomotor cerebellum in hummingbirds and zebra finches do not originate in the medial LM (as in pigeons) but instead largely arise from pretectal structures just medial, the nucleus laminaris precommissuralis and nucleus principalis precommissuralis. These species differences in projection patterns provide further evidence that optic flow circuits differ among bird species with distinct modes of flight.

Work loop dynamics of the pigeon (Columba livia) humerotriceps demonstrate potentially diverse roles for active wing morphing.

Control of wing shape is believed to be a key feature that allows most birds to produce aerodynamically efficient flight behaviors and high maneuverability. Anatomical organization of intrinsic wing muscles suggests specific roles for the different motor elements in wing shape modulation, but testing these hypothesized functions requires challenging measurements of muscle activation and strain patterns, and force dynamics. The wing muscles that have been best characterized 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 contractile cycle frequency of the humerotriceps, suggesting that this muscle may alter wing shape in diverse ways. To examine the multifunction potential of the humerotriceps, we developed an in situ work loop approach to measure how activation duration and contractile cycle frequency affected muscle work and power across the full range of activation onset times. The humerotriceps produced predominantly net negative power, likely due to relatively long stimulus durations, indicating that it absorbs work, but the work loop shapes also suggest varying degrees of elastic energy storage and release. The humerotriceps consistently exhibited positive and negative instantaneous power within a single contractile cycle, across all treatments. When combined with previous in vivo studies, our results indicate that both within and across contractile cycles, the humerotriceps can dynamically shift among roles of actuator, brake, and stiff or compliant spring, based on activation properties that vary with flight mode.

Visual-Cerebellar Pathways and Their Roles in the Control of Avian Flight.

In this paper, we review the connections and physiology of visual pathways to the cerebellum in birds and consider their role in flight. We emphasize that there are two visual pathways to the cerebellum. One is to the vestibulocerebellum (folia IXcd and X) that originates from two retinal-recipient nuclei that process optic flow: the nucleus of the basal optic root (nBOR) and the pretectal nucleus lentiformis mesencephali (LM). The second is to the oculomotor cerebellum (folia VI-VIII), which receives optic flow information, mainly from LM, but also local visual motion information from the optic tectum, and other visual information from the ventral lateral geniculate nucleus (Glv). The tectum, LM and Glv are all intimately connected with the pontine nuclei, which also project to the oculomotor cerebellum. We believe this rich integration of visual information in the cerebellum is important for analyzing motion parallax that occurs during flight. Finally, we extend upon a suggestion by Ibbotson (2017) that the hypertrophy that is observed in LM in hummingbirds might be due to an increase in the processing demands associated with the pathway to the oculomotor cerebellum as they fly through a cluttered environment while feeding.

Comparison of Visually Guided Flight in Insects and Birds.

Over the last half century, work with flies, bees, and moths have revealed a number of visual guidance strategies for controlling different aspects of flight. Some algorithms, such as the use of pattern velocity in forward flight, are employed by all insects studied so far, and are used to control multiple flight tasks such as regulation of speed, measurement of distance, and positioning through narrow passages. Although much attention has been devoted to long-range navigation and homing in birds, until recently, very little was known about how birds control flight in a moment-to-moment fashion. A bird that flies rapidly through dense foliage to land on a branch-as birds often do-engages in a veritable three-dimensional slalom, in which it has to continually dodge branches and leaves, and find, and possibly even plan a collision-free path to the goal in real time. Each mode of flight from take-off to goal could potentially involve a different visual guidance algorithm. Here, we briefly review strategies for visual guidance of flight in insects, synthesize recent work from short-range visual guidance in birds, and offer a general comparison between the two groups of organisms.

The Orientation of Visual Space from the Perspective of Hummingbirds.

Vision is a key component of hummingbird behavior. Hummingbirds hover in front of flowers, guide their bills into them for foraging, and maneuver backwards to undock from them. Capturing insects is also an important foraging strategy for most hummingbirds. However, little is known about the visual sensory specializations hummingbirds use to guide these two foraging strategies. We characterized the hummingbird visual field configuration, degree of eye movement, and orientation of the centers of acute vision. Hummingbirds had a relatively narrow binocular field (~30°) that extended above and behind their heads. Their blind area was also relatively narrow (~23°), which increased their visual coverage (about 98% of their celestial hemisphere). Additionally, eye movement amplitude was relatively low (~9°), so their ability to converge or diverge their eyes was limited. We confirmed that hummingbirds have two centers of acute vision: a fovea centralis, projecting laterally, and an area temporalis, projecting more frontally. This retinal configuration is similar to other predatory species, which may allow hummingbirds to enhance their success at preying on insects. However, there is no evidence that their temporal area could visualize the bill tip or that eye movements could compensate for this constraint. Therefore, guidance of precise bill position during the process of docking occurs via indirect cues or directly with low visual acuity despite having a temporal center of acute vision. The large visual coverage may favor the detection of predators and competitors even while docking into a flower. Overall, hummingbird visual configuration does not seem specialized for flower docking.

Morphology, muscle capacity, skill, and maneuvering ability in hummingbirds.

How does agility evolve? This question is challenging because natural movement has many degrees of freedom and can be influenced by multiple traits. We used computer vision to record thousands of translations, rotations, and turns from more than 200 hummingbirds from 25 species, revealing that distinct performance metrics are correlated and that species diverge in their maneuvering style. Our analysis demonstrates that the enhanced maneuverability of larger species is explained by their proportionately greater muscle capacity and lower wing loading. Fast acceleration maneuvers evolve by recruiting changes in muscle capacity, whereas fast rotations and sharp turns evolve by recruiting changes in wing morphology. Both species and individuals use turns that play to their strengths. These results demonstrate how both skill and biomechanical traits shape maneuvering behavior.

The retinal projection to the nucleus lentiformis mesencephali in zebra finch (Taeniopygia guttata) and Anna's hummingbird (Calypte anna).

In birds, the nucleus of the basal optic root (nBOR) and the nucleus lentiformis mesencephali (LM) are retinal recipient nuclei involved in the analysis of optic flow and the generation of the optokinetic response. In both pigeons and chickens, retinal inputs to the nBOR arise from displaced ganglion cells (DGCs), which are found at the margin of the inner nuclear and inner plexiform layers. The LM receives afferents from retinal ganglion cells, but whether DGCs also project to LM is a matter of debate. Previous work in chickens had concluded that DGCs do not project to LM, but a recent study in pigeons found that both retinal ganglion cells and DGCs project to LM. These findings leave open the question of whether there are species differences with respect to the DGC projection to LM. In the present study, we made small injections of retrograde tracer into the LM in a zebra finch and an Anna's hummingbird. In both cases, retrogradely labeled retinal ganglion cells and DGCs were observed. These results suggest that a retinal input to the LM arising from DGCs is characteristic of most, if not all, birds.