Hummingbirds control hovering flight by stabilizing visual motion

Abstract

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 ...

Optic flow stabilizes flight in ruby-throated hummingbirds

“…Our findings corroborate recent findings that Anna's hummingbirds control hovering position in response to projected visual motion (Goller and Altshuler, 2014). Our currently reported visual control of horizontal rotation and flight position in ruby-throated hummingbirds further supports the general view that birds and insects rely on both rotational and translational optic flow components to control flight maneuvers.…”

“…Therefore, both components likely serve to control and stabilize flight maneuvers. Previous findings that flight position in hummingbirds is controlled by optic flow (Goller and Altshuler, 2014) and that hawkmoths stabilize their flight position visually and possess visual interneurons sensitive to translational optic flow (Kern and Varju, 1998;Kern, 1998) corroborate our findings. However, our data cannot exclude the possibility that edge fixation on the retina, based on a vertical bar of the virtual surround employed in our experiments, may provide a second possible visual mechanism to control position.…”

“…Optic flow parameters, such as tau, representing time-to-contact, are also used by hawks and pigeons to land (Davies and Green, 1990) and by hummingbirds to approach feeders (Lee et al, 1993(Lee et al, , 1991. Recently, hummingbirds have also been shown to control hovering position using optic flow (Goller and Altshuler, 2014).…”

Flight mechanics and control of escape manoeuvres in hummingbirds II. Aerodynamic force production, flight control and performance limitations

“…For flying animals, the primary limiting factors of flight performance or manoeuvrability are arguably twofold: (1) attainable muscle mechanical power output (Altshuler et al, 2010a;Ellington, 1985Ellington, 1991Marden, 1994) associated with generation of aerodynamic manoeuvring forces and moments that create and maintain fast body movements, and (2) effective coordination of these movements using fast and accurate flightsensing and motor-control systems (Altshuler et al, 2012(Altshuler et al, , 2010bGoller and Altshuler, 2014;Iwaniuk and Wylie, 2007;Warrick et al, 2002). Limits of muscle mechanical power of hummingbirds have been extensively tested using load-lifting performance in short-burst flight (Altshuler et al, 2010a;Chai and Dudley, 1995;Marden, 1987Marden, , 1994.…”

Visual guidance of forward flight in hummingbirds reveals control based on image features instead of pattern velocity

“…More recent experiments demonstrate that pattern velocity does not affect the flight speed of budgerigars (12) in the same manner as it does flying insects (3, 13). Unlike bees and flies, the budgerigars increased their speed only slightly in response to large decreases in nasal-to-temporal pattern velocity, and they were not affected by large increases (12), demonstrating that birds do not adjust their flight speed to hold nasal-to-temporal pattern velocity constant.To determine if avian visual control of steering in flight differs from that of insects, we studied hummingbirds, agile fliers that perform rapid cruising flight as well as extended bouts of hover (14,15). We used an automated tracking system to record more than 3,100 flights of birds in free flight traversing a narrow tunnel where the wall patterns could be experimentally controlled (Fig.…”