Locomotor-driven oculomotor behavior that stabilizes gaze is timed to mid-tail region undulations during swimming in larval Xenopus - Archive ouverte HAL
Poster De Conférence Année : 2017

Locomotor-driven oculomotor behavior that stabilizes gaze is timed to mid-tail region undulations during swimming in larval Xenopus

Résumé

Body movements require compensatory eye adjustments to maintain a stable visual field. Our previous data from in vitro experiments on Xenopus laevis revealed that during locomotion, this gaze stabilization involved feedforward signaling from the spinal locomotor central pattern generator itself. By the past we showed that this locomotor efference copy signaling produces a bursting activity in horizontal extraocular motor nerves coupled with the bursting discharge in spinal ventral root nerves (VR). In order to produce compensatory conjugate eye movements during swimming, the discharge in lateral rectus (LR) motor nerve (and in the synergist medial rectus -MR- motor nerve) is in phase with the contralateral spinal rhythmic pattern. This spino-extraocular motor coupling originates from rostral spinal CPGs (until the 10th segment), that produce a robust undulatory swimming. However the kinematic of the tail undulation is the result of a multi-segmental wave of left-right alternative contraction. This multi-segmental alternative contraction is based on a rostro-caudal delay in the locomotor rhythm generated by the chain of spinal CPG. This delay determines the shape and the timing of the undulation of each part of the tail during swimming. Therefore the binary extraocular motor output has to be time-adjusted to the delayed multi-segment CPG locomotor rhythm in order to produce appropriate compensatory eye movements. This study aims to investigate the temporal calibration of the spino-extraocular motor command during multisegmental undulatory swimming sequences at larval stages 54-56. Video recordings (500fps) of head-fixed semi-intact preparations revealed that locomotor-induced conjugate eye-movements compensated perfectly the medio-caudal part of the tail (segments 15-20) and were in phase with the first rostral part of the tail (segments 1-7). Swimming sequences generated by these head fixed preparations provided a rostrocaudal undulation pattern comparable to those one observed during free swimming sequences. In vitro isolated semi-intact preparation of whole head and spinal cord were used to compare the eye movement with the extracellular activity of LR/MR and VR motor nerves during fictive swimming without visuo-vestibular inputs. Spinal VR discharge was recorded from segments 5, 12 and 20. Fictive swimming activity enhanced left-right movements of the left eye rhythmically coupled to the contralateral LR/MR motor nerve discharge. The rightward movement of the left eye was in phase with the discharge burst in the right LR motor nerve and the left VR 20 (as previously described in [1]) but out of phase with the left VR 5 (the most rostral tail regions). The perfusion of caudal spinal segments (from 12) with 20µM NMDA canceled the phase delay between LR, VR5, 12 and 20 motor nerves discharge bursts during fictive swimming. This last result suggests that if the rostral spinal segments are necessary to trigger the spino-extraocular command [1], the caudal spinal segments could be involved in the temporal adjustement of that spinal efference copy signal. These findings demonstrated that the locomotor feedforward spino-extraocular command produces conjugate eye movements calibrated to compensate the undulation pattern of the medial part of the tail. Previous biomechanical studies in tadpoles [2] showed that this tail region, where the fin is the highest, generates the maximum thrust during swimming sequences. Therefore the locomotor-induced oculomotor behavior would be constantly optimized to compensate the kinematic of the medial tail that produce the efficient straightforward swimming.
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hal-04724115 , version 1 (07-10-2024)

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  • HAL Id : hal-04724115 , version 1

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Julien Bacqué-Cazenave, G Courtand, Mathieu Beraneck, D Combes, F M Lambert. Locomotor-driven oculomotor behavior that stabilizes gaze is timed to mid-tail region undulations during swimming in larval Xenopus. 10th SFN Satellite Symposium on Motor Systems, Nov 2017, Washington, DC, United States. ⟨hal-04724115⟩
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