However, in contrast to the periods of stationary head “hold” phases that occur during walking ( Dunlap and Mowrer, 1930 Friedman, 1975 Frost, 1978), a pigeon's head never comes to a complete stop during landing flight. These in-flight head speed fluctuations are reminiscent of the head bobbing observed during walking in many birds. Similarly, by moving their head backwards and forwards relative to the body just before landing (but not after take-off), pigeons may use fluctuations in translational head speed relative to their surroundings to increase close-range perception of a landing site ( Green et al., 1994). Additionally, as optic flow increases, budgerigars, bees, moths, fruit flies, and blowflies reduce their flight speed to maintain an optic flow rate below a possible internal limit ( David, 1979 Srinivasan et al., 1996 Fry et al., 2009 Verspui and Gray, 2009 Bhagavatula et al., 2011 Kern et al., 2012). When flying down a corridor, budgerigars, and honeybees follow flight paths that balance left and right lateral optic flow induced by their translational movement ( Srinivasan et al., 1991 Bhagavatula et al., 2011). Translational optic flow appears to guide the flight behavior of several unrelated vertebrate and invertebrate species, indicating that it may provide a general visuomotor control stimulus. Consequently, understanding the relationship between sensory input and behavioral output is a key first step to elucidate behavioral and sensing-related adaptations, as well as how they interact, for robust flight control. Such features of flight behavior are, therefore, inferred to improve the quality of sensory perception in flies ( Nakayama, 1985 Zeil et al., 2008). By confining visual motion induced by self-rotation, or angular optic flow, to these rapid turns, a flying animal's course, speed, and distance information can be more easily extracted from translational optic flow that occurs during straight flight periods ( Land, 1999). For instance, fly flight is characterized by brief sharp turns alternated with periods of straight translational flight ( Schilstra and van Hateren, 1998). Sensory input clearly shapes behavior, but behavior can also shape sensory perception ( Zeil et al., 2008). However, the mechanisms by which sensory input is coupled to motor output for maneuvering flight in birds has been understudied compared to studies of avian functional anatomy, neural organization and sensory neurophysiology (for review, see Zeigler and Bischof, 1993). Such aerial maneuverability requires rapid sensory integration with motor control of the wings, body, and tail. The ability to maneuver, turn, and maintain stable flight has been critical to the evolutionary diversification and success of flying animals. Strong similarities between the sensory flight control of birds and insects may also inspire novel designs of robust controllers for human-engineered autonomous aerial vehicles. The control of head motion to stabilize a pigeon's gaze may therefore facilitate extraction of important motion cues, in addition to offering mechanisms for controlling body and wing movements. Visual cues inferred from head saccades correlate with changes in flight trajectory whereas the magnitude of neck bending predicts angular changes in body position. We observe that periods of angular head stabilization alternate with rapid head repositioning movements (head saccades), and confirm that control of head motion is decoupled from aerodynamic and inertial forces acting on the bird's continuously rotating body during turning flapping flight. Based on previous observations that the eyes of pigeons remain at relatively fixed orientations within the head during flight, we test potential sensory control inputs derived from head and body movements during 90° aerial turns.
Following from studies of visual and cervical feedback control of flight in insects, we investigate the role of head stabilization in providing feedback cues for controlling turning flight in pigeons. These principles indicate that robust solutions have evolved to meet complex behavioral challenges. Similar flight control principles operate across insect and vertebrate fliers.