Head Stabilization in the Pigeon: Role of Vision to Correct for Translational and Rotational Disturbances

Abstract

Stabilization of the head in animals with limited capacity to move their eyes is key to maintain a stable image on the retina. In many birds, including pigeons, a prominent example for the important role of head stabilization is the characteristic head-bobbing behavior observed during walking. Multimodal sensory feedback from the eyes, the vestibular system and proprioceptors in body and neck is required to control head stabilization. Here, we trained unrestrained pigeons (Columba livia) to stand on a perch that was sinusoidally moved with a motion platform along all three translational and three rotational degrees of freedom. We varied the frequency of the perturbation and we recorded the pigeons' responses under both light and dark conditions. Head, body, and platform movements were assessed with a high-speed motion capture system and the data were used to compute gain and phase of head and body movements in response to the perturbations. Comparing responses under dark and light conditions, we estimated the contribution of visual feedback to the control of the head. Our results show that the head followed the movement of the motion platform to a large extent during translations, but it was almost perfectly stabilized against rotations. Visual feedback only improved head stabilization during translations but not during rotations. The body compensated rotations around the forward-backward and the lateral axis, but did not contribute to head stabilization during translations and rotations around the vertical axis. From the results, we conclude that head stabilization in response to translations and rotations depends on different sensory feedback and that visual feedback plays only a limited role for head stabilization during standing.

How lovebirds maneuver through lateral gusts with minimal visual information

“…Indeed, both the vestibulocollic and the cervicocollic reflex-which remained functional in the dark-underpin active head stabilization in vertebrates (6,14). These findings are consistent with reports that body-fixed pigeons (15), free-standing pigeons (16), and hand-held owls (17) stabilize their head in the dark based on vestibular and proprioceptive feedback alone.…”

Mirror Self-Recognition in Pigeons: Beyond the Pass-or-Fail Criterion

“…Owing to the fact that the beak disappeared from the videos during most vertical foraging movement of the pigeons, it was not possible to track their beak, which might have provided direct information about head orientation. However, Theunissen and Troje (2017) demonstrated that pigeons often take a stable body position and compensate for the movement of environmental cues with head rotations. In the absence of moving cues, they usually keep their head-body position aligned.…”

What are birds looking at? A large-scale motion-capture system reveals the visual attention of freely- behaving pigeons

“…Another technique, and the one that we will adopt here, is to use a well-calibrated motion-capture system that can record the 3D coordinates of small re ective markers attached to a bird's head at a high temporal frequency and with submillimeter precision. Previous studies have employed this method to study pigeons' visual perception and 3D head orientations during perching (head stabilization) 41 , pecking (beak control) 42 , and walking (head bobbing) 43 . However, its use has been limited to relatively small laboratory spaces and the analysis of these relatively small-scaled individual behaviors.…”