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, 108 (27), 11291-6

Bat Wing Sensors Support Flight Control

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Bat Wing Sensors Support Flight Control

Susanne Sterbing-D'Angelo et al. Proc Natl Acad Sci U S A.

Abstract

Bats are the only mammals capable of powered flight, and they perform impressive aerial maneuvers like tight turns, hovering, and perching upside down. The bat wing contains five digits, and its specialized membrane is covered with stiff, microscopically small, domed hairs. We provide here unique empirical evidence that the tactile receptors associated with these hairs are involved in sensorimotor flight control by providing aerodynamic feedback. We found that neurons in bat primary somatosensory cortex respond with directional sensitivity to stimulation of the wing hairs with low-speed airflow. Wing hairs mostly preferred reversed airflow, which occurs under flight conditions when the airflow separates and vortices form. This finding suggests that the hairs act as an array of sensors to monitor flight speed and/or airflow conditions that indicate stall. Depilation of different functional regions of the bats' wing membrane altered the flight behavior in obstacle avoidance tasks by reducing aerial maneuverability, as indicated by decreased turning angles and increased flight speed.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Sensory wing hair before (A) and after (B and C) depilation. (A) Scanning electron microscope image from a domed hair located on the ventral trailing edge (location is marked by a gray circle in schematic to the Right) of Eptesicus fuscus. Note the calibration bar below the photomicrograph for reference. (Right) Schematic of the bat wing and its parts. (B and C) Examples of domes after depilation. Arrows point to the center of the domes from which the hair would normally protrude.
Fig. 2.
Fig. 2.
Cortical responses to airflow stimulation are diminished after depilation. The averaged poststimulus multiunit responses (time 0, end of air puff) to 10 air puff stimulations are shown for four different wing locations (see color-matched circles in bat schematic; open line, before depilation; filled area, after depilation). During the recording after hair removal, it was first tested whether the center of the tactile receptive field was still in the same location on the dorsal wing surface as before the depilation.
Fig. 3.
Fig. 3.
Directionality of responses to airflow in primary somatosensory cortex of Eptesicus fuscus. Top shows the directional responses of four multineuron clusters as polar plots. Airflow from each of the eight directions (every 45 °) was presented 20 times. The polar plots show the averages of the neuronal peak response, normalized to the peak. (Lower) Locations of the center of the receptive field (tip of arrow) for all tested neurons (n = 20). The arrows point in the direction of airflow that excites the neurons most at each location. The four colored arrows indicate the wing locations for the neuronal responses (Upper). Arrow thickness indicates the minimum–maximum ratio of the directional response strength. For example, a value of 0.5 indicates that for the nonpreferred direction the neuronal response was reduced by half compared with the preferred direction. Note that most neuronal clusters are tuned strongly with ratios between 0.5 and 1.
Fig. 4.
Fig. 4.
Flight experiments before and after wing hair removal in Eptesicus fuscus. The bat was trained to fly through a group of artificial trees to catch a tethered mealworm. Videos from two infrared-sensitive high-speed cameras were used to reconstruct the flight paths. (Left) Ten flight paths recorded over 10 trials before hair removal (viewed from top). (Right) Ten flight paths after removal of all tactile hairs along dorsal and ventral trailing edge (2-cm width of depilated wing membrane on each side). Note that the bat makes wider turns, i.e., the turn angle per frame decreased.
Fig. 5.
Fig. 5.
Flight experiments before and after wing hair removal in Carollia perspicillata. The bats had to fly through openings in two parallel nets to get a food reward (banana, Inset). (A) Flight speed was increased after hair removal along the trailing edge (black vs. blue line), (two animals, 117 trials, mean ± SE). Additional depilation of the leading edge (red) and midwing areas (green) did not further increase flight speed. (B) Conversely, the average turn angle of the bats decreased with wing hair depilation, indicating that their maneuverability was negatively affected (same trials as for A). (C) Flight speed vs. turn angle. After treatment the average maximum speed (mean ± SE) is increased and the maximum turn angle reduced. The bats generally make wider turns. (D) Flight speed vs. obstacle distance. The maximum distance to the obstacles is 16–25% greater after treatment.

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