A primal role for the vestibular sense in the development of coordinated locomotion

  1. David E Ehrlich
  2. David Schoppik  Is a corresponding author
  1. New York University School of Medicine, United States
7 figures, 2 videos, 3 tables and 1 additional file

Figures

Figure 1 with 3 supplements
Larvae climb using bodies and pectoral fins.

(A) Schematic of hydrostatic climbing mechanics. Like a rocket, a larva generates thrust in the direction it points (top), enabling it to generate upwards trajectories by rotating upwards to adopt …

https://doi.org/10.7554/eLife.45839.002
Figure 1—figure supplement 1
Larvae tend to sink between bouts.

(A) Schematic of hydrostatic forces acting on larvae absent lift during bouts (top) and between bouts (bottom). (B) Trajectory as a function of swim speed, plotted as means of equally-sized bins for …

https://doi.org/10.7554/eLife.45839.003
Figure 1—figure supplement 2
Posture as a function of time during bouts by control and finless siblings.

Data from individual bouts (gray lines) and their mean (black) were aligned to peak speed at time 0 and baseline subtracted at −0.75 s. (B) Angular speed as a function of time during bouts (bottom), …

https://doi.org/10.7554/eLife.45839.004
Figure 1—figure supplement 3
Basic swimming statistics are unaffected by fin amputation at 1 and 3 wpf.

(A–D) Mean maximum speed across bouts (A), mean net displacement (B), mean rate (C), and mean absolute body rotation (D) of swim bouts are plotted as thin lines by clutch (n = 6, eight larvae per) …

https://doi.org/10.7554/eLife.45839.005
Figure 2 with 2 supplements
Development of fin-body coordination.

(A) Schematic of fin-body coordination for climbing. Positive posture changes are paired with positive attack angles and negative body rotations with no attack angle, reflecting exclusion of the …

https://doi.org/10.7554/eLife.45839.008
Figure 2—figure supplement 1
Pectoral fins and bodies grow proportionally.

(A) Grayscale, dorsal-perspective photomicrographs of representative larvae at 1, 2, and 3 wpf, with rostrocaudal axis labeled (R–C). Pectoral fins are indicated with arrowhead. Gamma was adjusted …

https://doi.org/10.7554/eLife.45839.009
Figure 2—figure supplement 2
Clutch- and age-specific fin bias.

Attack angle as a function of posture change for individual clutches (columns) at each age (rows), plotted as means of equally-sized bins, superimposed with four parameter sigmoid fits. Empirical …

https://doi.org/10.7554/eLife.45839.010
Fin-body coordination is abolished by peripheral vestibular lesion.

(A) Representative lateral photomicrographs, one of a larva with typical development of utricular (anterior) otoliths (top, control: wild-type or heterozygous for otogelin) and another of its …

https://doi.org/10.7554/eLife.45839.012
Cerebellar lesion impairs fin-body coordination.

(A) Attack angle as a function of posture change for bouts by control larvae (602 bouts) and siblings with lesioned Purkinje cells (408 bouts). Data plotted as means of equally-sized bins (gray …

https://doi.org/10.7554/eLife.45839.015
Appendix 1—figure 1
A one-parameter control system captures fin-body coordination in silico.

(A) Circuit diagram to transform pitch-axis steering commands into climbing swims using the body and pectoral fins. Steering commands are defined by the direction of a target in egocentric …

https://doi.org/10.7554/eLife.45839.018
Appendix 1—figure 2
Effects of fin-body coordination on balance-effort trade-off.

(A) Trajectories (lines) and initial positions (dots) of bouts simulated with the control system in (A) at fin biases of 0, 0.74 (α^ at 1 wpf), 0.92 (α^ at 3 wpf), and 1.0, for 1000 larvae swimming …

https://doi.org/10.7554/eLife.45839.019
Appendix 1—figure 3
Steering cost functions computed from various formulations of effort.

(A) Cost as a function of fin bias for β (balance weights) of 0 (ochre, composed solely of effort), 0.2, 0.4, 0.6, 0.8, and 1 (green), for effort computed as the sum of absolute motor commands. (B) …

https://doi.org/10.7554/eLife.45839.020

Videos

Video 1
Lateral view of a freely-swimming, two wpf larva producing 4 bouts of upwards motion interleaved by periods of slow sinking.
https://doi.org/10.7554/eLife.45839.006
Video 2
View down the long axis of a freely-swimming, two wpf larva producing 5 bouts of upwards motion with visible pectoral fin abduction.
https://doi.org/10.7554/eLife.45839.007

Tables

Table 1
Empirical and simulated swimming properties and morphological measurements as a function of age.

Sigmoid parameters refer to the best-fit logistic function to attack angle vs. body rotation (Equation 1), comprising 4 degrees of freedom. ρ: Spearman’s correlation coefficient.

https://doi.org/10.7554/eLife.45839.011
VariableUnit4dpf1wpf2wpf3wpf
Mean attack angledeg0.871.024.788.11
R2 of trajectory and posture-0.860.910.780.66
Deviation from horizontaldeg13.9114.0811.9111.30
Swim bout peak speedmm/s11.213.613.414.1
Swim bout durations0.0930.0820.0870.106
Swim bout displacementmm1.241.291.241.43
Mean bout posture changedeg0.10−0.230.240.21
Standard deviation of bout posture changedeg2.211.841.842.10
ρ of attack angle and body rotation-0.3050.2690.3790.368
Proportion of climbs with trajectory > 20°-0.260.300.340.43
Body lengthmm4.184.265.577.92
Pectoral fin lengthmm0.410.420.610.90
Fin distance anterior to COMmm0.270.220.270.44
Sigmoid amplitude γmaxdeg19.2815.7114.3018.79
Sigmoid vertical location, γ0deg−3.00−1.59−3.72−3.56
Sigmoid horizontal location, rrestdeg−0.77−0.42−1.75−1.51
Sigmoid slope, kγmax/4-2.762.897.0312.01
Goodness-of-fit (R2) for 4-parameter sigmoid (k,γmax,γ0,rrest)-0.1950.1150.1130.087
Goodness-of-fit (R2) for 1-parameter sigmoid (k)-0.1930.1090.0920.086
Empirical fin bias, α^-0.730.740.880.92
Balance weight in cost function, β-0.120.120.180.32
Table 2
Morphology of otog-/- larvae and control siblings (otog+/- and otog+/+ with utricles).

Data listed as mean ± S.D.

https://doi.org/10.7554/eLife.45839.013
VariableUnitOtog-/-Control
Body lengthmm4.52 ± 0.324.53 ± 0.23
Pectoral fin lengthmm0.43 ± 0.030.42 ± 0.04
Pectoral fin length% body length9.6 ± 0.69.3 ± 0.8
Table 3
Swim bout properties for otog-/- and Tg(aldoca:GFF);Tg(UAS:KillerRed) larvae.

Data listed as mean ± S.D.

https://doi.org/10.7554/eLife.45839.014
VariableUnitOtog-/-, no utricleUtricle controlAldoca::KR lesionedAldoca::KR control
Maximum linear speedmm·s−112.4 ± 4.512.0 ± 4.310.7 ± 4.312.7 ± 4.5
Durations0.084 ± 0.0340.079 ± 0.0330.109 ± 0.0700.120 ± 0.051
Displacementmm1.23 ± 0.611.13 ± 0.541.25 ± 0.751.62 ± 0.71
Maximal pitch-axis angular speeddeg·s−198.7 ± 73.090.1 ± 69.084.4 ± 54.0100.6 ± 61.4
Inter-bout intervals1.22 ± 1.371.09 ± 1.032.09 ± 2.302.12 ± 2.80

Additional files

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