Temporal Relationship of Ocular and Tail Segmental Movements Underlying Locomotor-Induced Gaze Stabilization During Undulatory Swimming in Larval Xenopus.

Julien Bacqué-Cazenave,Mathieu Beraneck,Gilles Courtand,Denis Combes,François M Lambert

doi:10.3389/fncir.2018.00095

Abstract

In larval xenopus, locomotor-induced oculomotor behavior produces gaze-stabilizing eye movements to counteract the disruptive effects of tail undulation during swimming. While neuronal circuitries responsible for feed-forward intrinsic spino-extraocular signaling have recently been described, the resulting oculomotor behavior remains poorly understood. Conveying locomotor CPG efference copy, the spino-extraocular motor command coordinates the multi-segmental rostrocaudal spinal rhythmic activity with the extraocular motor activity. By recording sequences of xenopus tadpole free swimming, we quantified the temporal calibration of conjugate eye movements originating from spino-extraocular motor coupled activity during pre-metamorphic tail-based undulatory swimming. Our results show that eye movements are produced only during robust propulsive forward swimming activity and increase with the amplitude of tail movements. The use of larval isolated in vitro and semi-intact fixed head preparations revealed that spinal locomotor networks driving the rostral portion of the tail set the precise timing of the spino-extraocular motor coupling by adjusting the phase relationship between spinal segment and extraocular rhythmic activity with the swimming frequency. The resulting spinal-evoked oculomotor behavior produced conjugated eye movements that were in phase opposition with the mid-caudal part of the tail. This time adjustment is independent of locomotor activity in the more caudal spinal parts of the tail. Altogether our findings demonstrate that locomotor feed-forward spino-extraocular signaling produce conjugate eye movements that compensate specifically the undulation of the mid-caudal tail during active swimming. Finally, this study constitutes the first extensive behavioral quantification of spino-extraocular motor coupling, which sets the basis for understanding the mechanisms of locomotor-induced oculomotor behavior in larval frog.

Highlights

During locomotion, compensatory eye movements are produced to offset head/body movements, ensuring stable vision
We showed that locomotor-induced oculomotor behavior is only expressed during propulsive swimming behavior, elicited by an intrinsic feed-forward efference copy signaling that originates from rostral spinal motor networks, as previously described in vitro (Lambert et al, 2012)
Our results demonstrated that the feed-forward locomotor signal is timely set to generate a spino-extraocular motor coupling where the discharge bursts in extraocular motor nerves and in the contralateral 15–20th segmental spinal ventral roots are in phase during swimming episodes

Summary

Introduction

Compensatory eye movements are produced to offset head/body movements, ensuring stable vision. The swimming behavior can’t be explained with a restricted left-right alternating tail beat, but rather depends on a complex kinematic resulting from the sinewave-like undulation of the tail (Wassersug and von Seckendorf Hoff, 1985) Such undulatory movement is produced by a rostro-caudal sequential activation of multi-segmental spinal CPGs responsible for adjacent myotome contraction (Combes et al, 2004). The spino-extraocular motor command has to transform a multi-segmentally propagated CPG rhythmic pattern in a binary left-right alternating bursting discharge in synergistic LR/MR motor nerves. This raises the question as to which component of the tail movement is the locomotor efference copy temporally set, generating appropriate eye movements and compensating undulatory swimming?

Results

Discussion

Conclusion