On your marks, get set, look!
The director of a documentary will often use the unsteady images recorded by a handheld camera to give the viewer a sense of being in the thick of things. As we move about, the retinal image must be stabilized to allow adequate processing of visual information by the brain. The vestibular organ in the inner ear, which monitors movement and posture, plays an important role in this process. Sensory signals from this organ give rise to motor commands that induce compensatory movements of the eyes.
“Rapid and precise control of the eye muscles ensures that the eyes are held steady in space, so to speak,” says LMU neuroscientist Professor Hans Straka. Hence, the conversion of signals from the vestibular system into motor impulses for the ocular musculature has long been regarded as the primary mechanism involved in gaze stabilization during locomotion. Somewhat paradoxically, this inference is largely based on data obtained in experimental situations in which movements were not self-generated.
Direct stabilization of gaze
“However,” Straka points out, “whether we are moving or being moved does make a difference for signal processing in the brain.” Only during active locomotion do the brain and spinal cord produce the signals that coordinate contractions of the leg muscles, for example. So Straka and his team asked whether these signals are also conveyed to the eye muscles. As so-called “intrinsic efference copies”, they could be relayed internally, processed and used to stabilize gaze without any need for sensory input.
And if both systems are used, how might the two interact to control eye movements? To find out, the researchers performed studies, ranging from behavioral to cellular experiments, on tadpoles. Tadpoles use a stereotypic pattern of tail movements for swimming and, although immature, they possess fully functional eyes and vestibular organs. It turned out that intrinsic efference copies indeed activate eye movements, which coincide with, but are directed oppositely to, the undulating movements of the tail, to stabilize the gaze.
The team was able to show that the locomotory signals generated by spinal cord networks are transmitted directly to neurons in the brainstem, which then induce contractions of the ocular muscles. But what happens if the animals are passively rotated while swimming? “Signaling by the vestibular organ in response to the rotational movement is then actively suppressed,” says Straka. “So in this case too, the intrinsic efference copies are sufficient to ensure temporally and spatially appropriate eye movements.”
Compensating for sensory deficits
Strikingly, this inhibition of vestibular signaling is specific for passive rotation in the horizontal plane. Rotation in the vertical or lateral plane did not suppress the sensory signals. “Several issues remain be clarified in our animal model,” Straka explains. “But our findings could have implications for patients with certain disorders of the inner ear. In cooperation with the German Vertigo Center at the University Hospital in Grosshadern, we want to test whether the intrinsic signals from the spinal cord can compensate for sensory deficits resulting from unilateral loss of vestibular function.”
The project was sponsored by the Collaborative Research Center (SFB 870) “Assembly and Function of Neuronal Circuits in Sensory Processing“ (Current Biology, 26. July 2012) suwe