Bird flight is a remarkable adaptation that has allowed the approximately 10 000 extant species to colonize all terrestrial habitats on earth including high elevations, polar regions, distant islands, arid deserts, and many others. Birds exhibit numerous physiological and biomechanical adaptations for flight. Although bird flight is often studied at the level of aerodynamics, morphology, wingbeat kinematics, muscle activity, or sensory guidance independently, in reality these systems are naturally integrated. There has been an abundance of new studies in these mechanistic aspects of avian biology but comparatively less recent work on the physiological ecology of avian flight. Here we review research at the interface of the systems used in flight control and discuss several common themes. Modulation of aerodynamic forces to respond to different challenges is driven by three primary mechanisms: wing velocity about the shoulder, shape within the wing, and angle of attack. For birds that flap, the distinction between velocity and shape modulation synthesizes diverse studies in morphology, wing motion, and motor control. Recently developed tools for studying bird flight are influencing multiple areas of investigation, and in particular the role of sensory systems in flight control. How sensory information is transformed into motor commands in the avian brain remains, however, a largely unexplored frontier.

Relatively little is known about how sensory information is used for controlling flight in birds. A powerful method is to immerse an animal in a dynamic virtual reality environment to examine behavioral responses. Here, we investigated the role of vision during free-flight hovering in hummingbirds to determine how optic flowimage movement across the retina-is used to control body position. We filmed hummingbirds hovering in front of a projection screen with the prediction that projecting moving patterns would disrupt hovering stability but stationary patterns would allow the hummingbird to stabilize position. When hovering in the presence of moving gratings and spirals, hummingbirds lost positional stability and responded to the specific orientation of the moving visual stimulus. There was no loss of stability with stationary versions of the same stimulus patterns. When exposed to a single stimulus many times or to a weakened stimulus that combined a moving spiral with a stationary checkerboard, the response to looming motion declined. However, even minimal visual motion was sufficient to cause a loss of positional stability despite prominent stationary features. Collectively, these experiments demonstrate that hummingbirds control hovering position by stabilizing motions in their visual field. The high sensitivity and persistence of this disruptive response is surprising, given that the hummingbird brain is highly specialized for sensory processing and spatial mapping, providing other potential mechanisms for controlling position. T o precisely control their motion through the air, flying animals have evolved specialized sensory structures and associated neural architecture. Neural specializations provide hypotheses for what senses are most important to a given taxon, and although flight control has been studied extensively in insects (1), birds have until recently received limited attention. Birds have large regions of the brain dedicated to visual processing, suggesting parallels with insects, such as a leading role for optic flow in controlling flight paths (2, 3). It has recently been demonstrated that birds exhibit visually mediated position control much like bees (4, 5), even though they have complex spatial mapping in the hippocampal formation (6), and a much larger brain for interpreting visual input and dynamically integrating vision with proprioceptive and vestibular feedback (7-9).In birds and mammals, the visual information from the eyes is divided into three separate pathways that each process a subset of motions or visual features (10). Two of these pathways, named the accessory optic system and tectofugal pathways in birds, each process a single type of motion: (i) self-or ego-motion, which is the motion produced when an observer moves relative to their environment; and (ii) object motion, when visual features move relative to the observer (2). Using the same retinal information, the visual system of a flying hummingbird must separate motions arising from the bird moving through foliage toward a ...

Neurons in animal visual systems that respond to global optic flow exhibit selectivity for motion direction and/or velocity. The avian lentiformis mesencephali (LM), known in mammals as the nucleus of the optic tract (NOT), is a key nucleus for global motion processing [1-4]. In all animals tested, it has been found that the majority of LM and NOT neurons are tuned to temporo-nasal (back-to-front) motion [4-11]. Moreover, the monocular gain of the optokinetic response is higher in this direction, compared to naso-temporal (front-to-back) motion [12, 13]. Hummingbirds are sensitive to small visual perturbations while hovering, and they drift to compensate for optic flow in all directions [14]. Interestingly, the LM, but not other visual nuclei, is hypertrophied in hummingbirds relative to other birds [15], which suggests enhanced perception of global visual motion. Using extracellular recording techniques, we found that there is a uniform distribution of preferred directions in the LM in Anna's hummingbirds, whereas zebra finch and pigeon LM populations, as in other tetrapods, show a strong bias toward temporo-nasal motion. Furthermore, LM and NOT neurons are generally classified as tuned to "fast" or "slow" motion [10, 16, 17], and we predicted that most neurons would be tuned to slow visual motion as an adaptation for slow hovering. However, we found the opposite result: most hummingbird LM neurons are tuned to fast pattern velocities, compared to zebra finches and pigeons. Collectively, these results suggest a role in rapid responses during hovering, as well as in velocity control and collision avoidance during forward flight of hummingbirds.

BackgroundAvian collisions with man-made objects and vehicles (e.g., buildings, cars, airplanes, power lines) have increased recently. Lights have been proposed to alert birds and minimize the chances of collisions, but it is challenging to choose lights that are tuned to the avian eye and can also lead to avoidance given the differences between human and avian vision. We propose a choice test to address this problem by first identifying wavelengths of light that would over-stimulate the retina using species-specific perceptual models and by then assessing the avoidance/attraction responses of brown-headed cowbirds to these lights during daytime using a behavioral assay.MethodsWe used perceptual models to estimate wavelength-specific light emitting diode (LED) lights with high chromatic contrast. The behavioral assay consisted of an arena where the bird moved in a single direction and was forced to make a choice (right/left) using a single-choice design (one side with the light on, the other with the light off) under diurnal light conditions.ResultsFirst, we identified lights with high saliency from the cowbird visual perspective: LED lights with peaks at 380 nm (ultraviolet), 470 nm (blue), 525 nm (green), 630 nm (red), and broad-spectrum (white) LED lights. Second, we found that cowbirds significantly avoided LED lights with peaks at 470 and 630 nm, but did not avoid or prefer LED lights with peaks at 380 and 525 nm or white lights.DiscussionThe two lights avoided had the highest chromatic contrast but relatively lower levels of achromatic contrast. Our approach can optimize limited resources to narrow down wavelengths of light with high visual saliency for a target species leading to avoidance. These lights can be used as candidates for visual deterrents to reduce collisions with man-made objects and vehicles.

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