Lambert FM et al. (2020), Stabilization of Gaze during Early Xenopus Deve...

XB-ART-56632

Curr Biol 2020 Feb 24;304:746-753.e4. doi: 10.1016/j.cub.2019.12.047.

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Stabilization of Gaze during Early Xenopus Development by Swimming-Related Utricular Signals.

Lambert FM , Bacqué-Cazenave J , Le Seach A , Arama J , Courtand G , Tagliabue M , Eskiizmirliler S , Straka H , Beraneck M .

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Locomotor maturation requires concurrent gaze stabilization improvement for maintaining visual acuity [1, 2]. The capacity to stabilize gaze, in particular in small aquatic vertebrates where coordinated locomotor activity appears very early, is determined by assembly and functional maturation of inner ear structures and associated sensory-motor circuitries [3-7]. Whereas utriculo-ocular reflexes become functional immediately after hatching [8, 9], semicircular canal-dependent vestibulo-ocular reflexes (VORs) appear later [10]. Thus, small semicircular canals are unable to detect swimming-related head oscillations, despite the fact that corresponding acceleration components are well-suited to trigger an angular VOR [11]. This leaves the utricle as the sole vestibular origin for swimming-related compensatory eye movements [12, 13]. We report a remarkable ontogenetic plasticity of swimming-related head kinematics and vestibular end organ recruitment in Xenopus tadpoles with beneficial consequences for gaze-stabilization. Swimming of older larvae generates sinusoidal head undulations with small, similar curvature angles on the left and right side that optimally activate horizontal semicircular canals. Young larvae swimming causes left-right head undulations with narrow curvatures and strong, bilaterally dissimilar centripetal acceleration components well suited to activate utricular hair cells and to substitute the absent semicircular canal function at this stage. The capacity of utricular signals to supplant semicircular canal function was confirmed by recordings of eye movements and extraocular motoneurons during off-center rotations in control and semicircular canal-deficient tadpoles. Strong alternating curvature angles and thus linear acceleration profiles during swimming in young larvae therefore represents a technically elegant solution to compensate for the incapacity of small semicircular canals to detect angular acceleration components.

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GO keywords: swimming behavior

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	Graphical Abstract
	Figure 1Compensatory Eye Movements During Free Swimming (A) Frame-by-frame motion trajectory of larval swimming at stage 47 (A1) and 57 (A2) obtained from high-speed videos. (B and C) Representative examples of multiple cycles (B) and average (±SD, shaded area) over a single cycle (C) of swimming-related head and concurrent compensatory movements of the left (Le, green) and right (Ri, blue) eye at stage 47 (B1 and C1) and 57 (B2 and C2). (D and E) Scatterplots of eye excursion angle (D) and eye-in-head ratio (excursion angles of eye/head, E) as function of the head excursion angle. (F and G) Mean swim speed as function of body length (F) at stage 47 (n = 25) and stage 57 (n = 27) and distribution of mean (±SD) swim speeds (G); ∗∗∗p < 0.001 (Mann-Whitney U test). (H and I) Distribution of absolute (H) and normalized average swim speed (I; relative to average swim speed, see G).
	Figure 2Comparison of Head Motion Trajectories (A and B) Head trajectory (A1 and B1, see Videos S1 and S2); magnified views of the head turn (A2 and B2) over a period of 60 ms (dashed rectangular area marked with ∗ in A1 and B1) during swimming of stage 47 (A) and 57 (B) tadpoles; note that the displacement of the inner side of the head turn (green) causes the head movements (interconnecting lines between the eyes in A2 and B2) to be more accentuated in younger animals; frame-by-frame position of eyeballs and inner ears at the peak of the head turn (A3 and B3) indicate the curvature and the direction (dashed lines) on the inner ear from the first to the last image of the 60 ms time window.
	Figure 3Influence of Rotation Axis Position on Eye Movements in Tadpoles with Intact, Pharmacologically Impaired, or Semicircular Canal-Deficient Inner Ears. (A) Movement of the left (dark traces) and right (light traces) eye at stage 47 during horizontal rotation with the vertical axis in the center (A1, blue), left-right linear translation (A2, pink; see Video S3), and during off-center (left-out centered in A3; Le-out, purple; see Video S4) under control condition (blue traces) and after injection of 0.5% MS-222 into both inner ears (red traces); note that the robust conjugate compensatory eye movements during translation (A2) and off-center rotation (A3) were completely abolished by the local anesthetic (see also Figure S4).(B and C) Four successive motion cycles (B) and average over a single cycle (mean ± SEM, C) of the left (dark traces) and right eye (light traces) during horizontal rotation with the vertical axis in the center (B1 and C1, blue), left-right linear translation (B2 and C2, pink), and during off-center (B3 and C3; Le-out, purple) in a semicircular canal-deficient stage 50 tadpole (n = 5); note the absence of eye movements during centered vertical-axis rotations and their persistence during off-center rotations and translations (see also Figure S4).
	Figure 4Developmental Plasticity of Locomotor Dynamics and Corresponding Inner Ear Organ Recruitment A) Presumed differential activation of the utricle (utr.), semicircular canals (can.), VORs, and spinal feedforward efference copies (Sp. ffwd) during swimming at stage 47 and 57 (upper row) in correspondence with changes of head centripetal acceleration and curvature profiles (lower rows). (B) Swim pattern and spatial displacement of the bilateral utricle during the different swimming-related head rotations at stage 47 (left) and stage 57 (right) between time n-1 point (tn-1 in gray) and time n point (tn in black); linear, utricular (blue solid arrows); and angular, semicircular canal acceleration components (red solid arrow) are indicated; magenta dashed arrows represent the resulting centripetal linear component during out-axis rotation. α, Θ, angular displacement between tn-1 and tn.
	Figure S1. Morphometric analysis of anatomical features and off-line calculation of head motion kinematic parameters. Related to STAR Methods. (A) Images depicting dorsal (left) and ventral views (middle, right) of a stage 57 larvae with outlined locations and measured or triangulated relative distances between eyes (green), heart (orange) and otic capsules (OC, magenta); anatomical markers served subsequently as landmarks for tracking the head motion during swimming. (B) Scaled drawings of the head/body at stage 47 and 57 (left) and morphometric ratios of measured or calculated anatomical markers (right); note that despite size differences, relative distances between eyes, heart, OC remain constant during development, ns, not significant (Mann-Whitney U-test). (C) Schematic of the set-up for high speed (500 fps) video recordings of free swimming. (D) Ventral view of video imaged swimming of a stage 57 tadpole depicting the tracked trajectories of both eyes (green) and the triangulated heart (orange) and OCs (magenta) at the time point tn. (E) Schematic summarizing the trajectory of the triangulated motion of the OC along with the direction and size of the forward, lateral, centripetal and angular acceleration vectors calculated from the displacement (disp.) between time point tn-1 (gray) and time point tn (black); , angular displacement.
	Figure S2. Comparison of swimming speed. Related to Figure 2. (A, B and C) Instantaneous swimming speed (A1 and A2) obtained from the extracted trajectory of the body center (heart, B1 and B2) and extracted horizontal head movements during swimming (C1 and C2). (D and E) Sequence ranked mean swim speed (±SD; D) and velocity of the inner side of the head turn on the left (solid lines) and right (dotted lines) side (E). (F) Distribution of the Delta curvature (left - right inner ear curvature) obtained from all swimming sequences; **** p < 0.0001 (Kolmogorov-Smirnov test).
	Figure S3. Magnitudes and distribution of head acceleration components during swimming. Related to Figure 2. (A and B) Scatter plots (A) and relative distributions (B) of forward linear (A1 and B1), lateral linear (A2 and B2), angular (A3 and B3) and centripetal linear (A4 and B4) acceleration components, calculated for the OC at the peak curvature of each swimming cycle; note the marked difference in the distribution profile of centripetal linear acceleration components of stage 47 and 57 tadpoles.
	Figure S4. Eye movements and extraocular motor discharge under control conditions and after impairment of the sensory transduction. Related to Figure 3. (A) Phase relation of cyclic eye movements during translation and rotational motion around off-center axes positioned on the left (le-out) and right side (ri-out) at stage 47 under control condition. (B, C and D) Movement of the left (dark traces) and right (light traces) eye at stage 47 during horizontal rotation with the vertical axis off-center (Ri-out, orange) under control condition (B) and after injection of 0.5% MS-222 into both inner ears (C); note that eye movements were completely abolished by the local anesthetic. See supplemental videos 3A2 and A3. (D) Average over a single cycle (mean ±SEM) of the left and right eye during translational motion (D1) and horizontal rotation with the position of the off-center vertical axis left-out (D2) or right-out (D3) before (blue traces) and after injection of 0.5% MS-222 (n = 6) into both inner ears on stage 47 tadpoles; note the significant reduction of the respective eye motion amplitudes after the injection (D4); * p < 0.05, *** p < 0.001 (MannWhitney U-test); (E) Four successive motion cycles (E1) and average over a single cycle (mean ±SEM, E2) of the left and right eyes during horizontal rotation with the vertical axis off-center (Ri-out) in semicircular canal-deficient stage 50 tadpoles (n = 5); note the persistence of eye movements. (F) Schematic of a semi-intact stage 50 whole-head preparation of larval Xenopus (F1) depicting abducens motor nerve recordings during horizontal rotation around a vertical axis in the center (black) or off-center on the left (Le-out, purple) or right side (Ri-out, orange); single sweeps of abducens nerve discharge during sinusoidal horizontal rotation (blue trace) around the le-out axis (top, purple), center (middle, black), and ri-out axis (bottom, orange) at 1 Hz and ±120°/s peak velocity (top traces in F2); average abducens nerve firing rate modulation (±SEM, shaded areas, bottom traces in F2) over a single motion cycle (blue trace) and firing rate (mean ±SEM) as function of peak head velocity (F3) during 1 Hz rotation around the three different axes; note that the LR nerve spike discharge, phase-timed with contraversive head peak velocity, was modulated during rotations (1 Hz; ±30 - 240°/s) around on- and off-center axes; however, peak firing rates were consistently larger for rotations around an eccentric compared to the centered axis with larger responses following rotations around the eccentric axis contralateral to the recorded LR nerve.