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

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.