Conservation of locomotion-induced oculomotor activity through evolution in higher tetrapods

Abstract

Efference copies are neural replicas of motor outputs used to anticipate the sensory consequences of a self-generated motor action or to coordinate neural networks involved in distinct motor behaviors1. An established example of this motor-to-motor coupling is the efference copy of the propulsive motor command that supplements classical visuo-vestibular reflexes to ensure gaze stabilization during amphibian larval locomotion2. Such feedforward replica from spinal pattern-generating circuits produces a spino-extraocular motor coupled activity that evokes eye movements, spatio-temporally coordinated to tail undulation independently of any sensory signal3,4. Exploiting the evolutionary-development characteristic of the frog1, studies in metamorphing Xenopus demonstrated the persistence of this spino-extraocular motor command in adults, and its developmental adaptation to tetrapodal locomotion5,6. Here, we demonstrate for the first time the existence of a comparable locomotor-to-ocular motor coupling in the mouse. In neonates, ex vivo nerve recordings from brainstem-spinal cord preparation reveals a spino-extraocular motor coupled activity similar to the one described in Xenopus. In adult mice, trans-synaptic rabies injection in lateral rectus eye muscle labels cervical spinal cord neurons projecting directly to abducens motor neurons. Finally, treadmill-elicited locomotion in decerebrated preparations7 evokes rhythmic eye movements in synchrony with the limb gait pattern. Overall, our data are evidence for the conservation of locomotor-induced eye movements in higher tetrapods. Thus, in mammals as in amphibians, during locomotion CPG-efference copy feedforward signals might interact with sensory feedback to ensure efficient gaze control. HighlightsO_LISpino-extraocular motor coupling is evidenced from newborn mice ex vivo preparations C_LIO_LIAdult decerebrated mice exhibit conjugated rhythmic eye movements during treadmill locomotion C_LIO_LILocomotor-induced oculomotor activity occurs in absence of visuo-vestibular inputs C_LIO_LIConserved CPG-based efference copy signal in vertebrates with common features. C_LI eTOC blurbWe report a functional coupling between spinal locomotor and oculomotor networks in the mouse, similar to the one previously described in Amphibians. This is the first evidence for the direct contribution of locomotor networks to gaze control in mammals, suggesting a conservation of the spino-extraocular coupling in higher tetrapods during sustained locomotion.