Conservation of locomotion-induced oculomotor activity through evolution in mammals

• Published in: Current biology 2022-01, Vol.32 (2), p.453-461.e4
• Main Authors: França de Barros, Filipa, Bacqué-Cazenave, Julien, Taillebuis, Coralie, Courtand, Gilles, Manuel, Marin, Bras, Hélène, Tagliabue, Michele, Combes, Denis, Lambert, François M., Beraneck, Mathieu
• Format: Article
• Language: English
• Subjects: Animals; Central pattern generators; efference copy; Eye Movements; functional coupling; gaze stabilization; Life Sciences; locomotion; Locomotion - physiology; locomotor; Mammals; Mice; Motor Neurons - physiology; Neurons and Cognition; oculomotor; Reflex, Vestibulo-Ocular - physiology; Spinal Cord - physiology; vestibular; Xenopus laevis - physiology
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.11.022

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 behaviors.1 An established example of this motor-to-motor coupling is the efference copy of the propulsive motor command, which supplements classical visuo-vestibular reflexes to ensure gaze stabilization during amphibian larval locomotion.2 Such feedforward replica of spinal pattern-generating circuits produces a spino-extraocular motor coupled activity that evokes eye movements, spatiotemporally coordinated to tail undulation independently of any sensory signal.3,4 Exploiting the developmental stages of the frog,1 studies in metamorphing Xenopus demonstrated the persistence of this spino-extraocular motor command in adults and its developmental adaptation to tetrapodal locomotion.5,6 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 of brainstem-spinal cord preparations reveal a spino-extraocular motor coupled activity similar to the one described in Xenopus. In adult mice, trans-synaptic rabies virus injections in lateral rectus eye muscle label cervical spinal cord neurons closely connected 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 vertebrate lineages. Thus, in mammals as in amphibians, CPG-efference copy feedforward signals might interact with sensory feedback to ensure efficient gaze control during locomotion. •Spino-extraocular motor coupling is evidenced from newborn mice ex vivo preparation•Adult decerebrated mice exhibit conjugated rhythmic eye movements during locomotion•Locomotor-induced oculomotor activity occurs in absence of visuo-vestibular inputs•Conserved CPG-based efference copy signal in vertebrates with common features França de Barros et al. report a functional coupling between spinal locomotor and oculomotor networks in mice, similar to the one previously described in amphibians. This is the first evidence of the direct contribution of locomotor networks to gaze control in mammals, suggesting a conservation of the spino-extraocular coupling through evolution.