The Organization of Central Retinal Projections in Anna's Hummingbirds (Calypte anna) and Zebra Finches (Taeniopygia castanotis).

Hummingbirds (family Trochilidae) are easily recognized due to their unique ability to hover. Critical to hovering flight is head and body stabilization. In birds, stabilization during flight is mediated, among other things, by the detection of optic flow, the motion that occurs across the entire retina during self-motion.

Wing extension-flexion coupled aeroelastic effects improve avian gliding performance.

During flight, birds instigate remarkably large changes in wing shape, commonly termed 'wing morphing'. These changes in shape, particularly extension-flexion, have been well documented to influence the production of aerodynamic forces. However, it is unknown how wing stiffness changes as a result of the structural rearrangements needed for morphing.

Understanding mechanisms of avian flight by integrating observations with tests of competing hypotheses.

A long-standing problem in the study of avian flight is determining how biomechanics and physiology are associated with behaviour, ecological interactions and evolution. In some avian clades, flight mechanisms are strongly linked to ecology. Hummingbirds, for example, exhibit traits that support both hovering flight and nectar foraging.

Hummingbirds use compensatory eye movements to stabilize both rotational and translational visual motion.

To maintain stable vision, behaving animals make compensatory eye movements in response to image slip, a reflex known as the optokinetic response (OKR). Although OKR has been studied in several avian species, eye movements during flight are expected to be minimal. This is because vertebrates with laterally placed eyes typically show weak OKR to nasal-to-temporal motion (NT), which simulates typical forward locomotion, compared with temporal-to-nasal motion (TN), which simulates atypical backward locomotion.

Encoding of Global Visual Motion in the Avian Pretectum Shifts from a Bias for Temporal-to-Nasal Selectivity to Omnidirectional Excitation across Speeds.

The pretectum of vertebrates contains neurons responsive to global visual motion. These signals are sent to the cerebellum, forming a subcortical pathway for processing optic flow. Global motion neurons exhibit selectivity for both direction and speed, but this is usually assessed by first determining direction preference at intermediate velocity (16-32°/s) and then assessing speed tuning at the preferred direction.

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.

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.

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).

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).

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.

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 (fructose-bisphosphatase 2), which encodes a gluconeogenic muscle enzyme, was lost during a time period when hovering flight evolved.

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. The midbrain circuitry for optic flow is highly conserved in vertebrates, and these neurons show similar response properties across tetrapods. These neurons have large receptive fields and exhibit both direction and velocity selectivity in response to large moving stimuli.

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.

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.

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

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 () 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.

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.

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 () 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.

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.

Work loop dynamics of the pigeon () 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 ().

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).

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.

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.

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.

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.