Inflight head stabilization associated with wingbeat cycle and sonar emissions in the Egyptian fruit bat

Sensory processing of environmental stimuli during locomotion is critical for the successful execution of goal-directed behaviors and navigating around obstacles. The outcome of these sensorimotor processes can be challenged by head movements that perturb the sensory coordinate frames directing behaviors. In the case of visually-guided behaviors, visual gaze stabilization results from the integrated activity of the vestibuloocular reflex and motor efference copy originating within circuits driving locomotor behavior. A recent videographic study showed that echolocating bats exhibit inflight head stabilization during a target identification and landing task, though compensatory timing of the bats’ sonar signals was not reported. In the present investigation we tested hypotheses that head stabilization is more broadly implemented during epochs of exploratory flight, and is temporally associated with emitted sonar signals, which would optimize acoustic gaze. This was achieved by measuring head and body kinematics with motion sensors secured to the head and body of free-flying Egyptian fruit bats. These devices were integrated with ultrasonic microphones to record the bat’s sonar emissions and elucidate their temporal association with periods of head stabilization. Head accelerations in the Earth-vertical axis were asymmetric with respect to wing downbeat and upbeat relative to body accelerations. This indicated that inflight head and body accelerations were uncoupled, outcomes consistent with the implementation of head movements that limit vertical acceleration during wing downbeat. Furthermore, sonar emissions during stable flight occurred most often during wing downbeat and head stabilization, supporting the conclusion that head stabilization behavior optimized sonar gaze and environmental interrogation via echolocation.Summary statementDirect measurements of head and body kinematics from affixed motion sensors revealed head stabilization behaviors during exploratory flights in bats. Most sonar emissions were temporally correlated with this behavior, thereby contributing to the optimization of acoustic gaze.

Head stabilization in small vertebrates that run at high frequencies with a sprawled posture

Small animals face a large challenge when running. A stable head is key to maintenance of a stable gaze and a good sense of self-motion and spatial awareness. However, trunk undulations caused by the cyclic limb movements result in involuntary head movements. Hence, the head needs to be stabilized. Humans are capable of stabilizing their head up to 2–3 Hz, but small animals run at cycle frequencies that are up to six times higher. We wondered how natural selection has adapted their head stabilization control. We observed that the relative contributions of vision, on the one hand, and vestibular perception and proprioception, on the other hand, remain the same when lizards undergo fast or slow body undulations in an experimental set-up. Lizards also maintain a short phase lag at both low and high undulation frequencies. Hence, we found no indication that they use a different control mechanism at high frequencies. Instead, head stabilization probably remains possible owing to faster reflex pathways and a lower head inertia. Hence, the intrinsic physical and neurological characteristics of lizards seem to be sufficient to enable head stabilization at high frequencies, obviating the need for evolutionary adaptation of the control pathways. These properties are not unique to lizards and might, therefore, also facilitate head stabilization at high frequencies in other small, fast animals.

On the mechanical contribution of head stabilization to passive dynamics of anthropometric walkers

During the steady gait, humans stabilize their head around the vertical orientation. Although there are sensori-cognitive explanations for this phenomenon, its mechanical effect on the body dynamics remains unexplored. In this study, we take profit from the similarities that human steady gait shares with the locomotion of passive-dynamics robots. We introduce a simplified anthropometric 2D model to reproduce a broad walking dynamics. In a previous study, we showed heuristically that the presence of a stabilized head–neck system has a significant influence on the dynamics of walking. This article gives new insights that lead to understanding this mechanical effect. In particular, we introduce an original cart upper-body model that allows to better understand the mechanical interest of head stabilization when walking, and we study how this effect is sensitive to the choice of control parameters.