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Research ArticleResearch Article: Methods/New Tools, Sensory and Motor Systems

Whole-Body Imaging of Neural and Muscle Activity during Behavior in Hydra vulgaris: Effect of Osmolarity on Contraction Bursts

Wataru Yamamoto and Rafael Yuste
eNeuro 22 July 2020, 7 (4) ENEURO.0539-19.2020; DOI: https://doi.org/10.1523/ENEURO.0539-19.2020
Wataru Yamamoto
1Neurotechnology Center, Department Biological Sciences, Columbia University, New York, NY 10027
1Neurotechnology Center, Department Biological Sciences, Columbia University, New York, NY 10027
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Rafael Yuste
1Neurotechnology Center, Department Biological Sciences, Columbia University, New York, NY 10027
2Marine Biological Laboratory, Woods Hole, MA 02543
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    Figure 1.

    Effect of experimental conditions on contractions and locomotion behavior. Data from mounted preparations in A–C and from 1-h freely moving Hydra in D–F. A, Upper images, Changes in body length during longitudinal contractions. Lower images, Foot detachment. Scale bar, 500 μm. Number of contractions (B) and foot detachments (C) were counted. D, Upper images depict changes in body length during longitudinal contractions. Lower images depict foot detachment followed by locomotion. Scale bar, 1 mm. Number of contractions (E) and foot detachment/locomotion (F) were counted. The four conditions used were food (Food), osmolarity (Osmo), size (Size), and temperature (Temp). Control medium (ctr). Error bars shown as mean ± SEM, with symbol marks denoting data points from individual Hydra (N = 9–16 for B, C; N = 15–30 for E, F). Tukey’s multiple comparisons tests were performed following one-way ANOVA for osmolarity experiment, and Student’s t test was performed for others: ns ≥ 0.05; *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001.

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    Figure 2.

    Effect of experimental conditions on ectoderm and endoderm muscle activity. A, upper images, Measurements of contractions in Hydra expressing GCaMP6s in ectoderm muscle. Lower images, contractions in Hydra expressing GCaMP6s in endoderm muscle. Scale bar, 500 μm. B, Schematic summarizing steps to detect peaks of CB pulses from raw traces extracted from 2-h calcium imaging movies. RP1 pulses were not present in muscle activity. C–H, Each type of response was analyzed with four variables: (C) ectoderm CB pulse number; (D) endoderm CB pulse number; (E) ectoderm CB total time; (F) endoderm CB total time; (G) ectoderm CB total time; (H) endoderm CB total time. The four conditions used were food (Food), osmolarity (Osmo), size (Size), and temperature (Temp). Control medium (ctr). Error bars are shown as the mean ± SEM, with symbol marks denoting data points from individual Hydra (N = 3–6). Tukey’s multiple comparisons tests were performed following one-way ANOVA for osmolarity experiment, and Student’s t test was performed for others: ns ≥ 0.05; *p < 0.05.

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    Figure 3.

    Effect of experimental conditions on neuronal activity. A, upper images, Activation of CB neurons. Lower images, Activation of RP1 neurons. Scale bar, 500 μm. B, Schematic summarizing steps to detect peaks of CB and RP1 pulses from raw traces extracted from 2-h calcium imaging. C–H, Analysis of parameters: (C) CB pulse number; (D) RP1 pulse number; (E) CB total time; (F) RP1 total time; (G) CB pulse frequency; (H) RP1 pulse frequency. The four conditions used were food (Food), osmolarity (Osmo), size (Size), and temperature (Temp). Control medium (ctr). Error bars are shown as the mean ± SEM, with symbol marks denoting data points from individual Hydra (N = 3–8). Tukey’s multiple comparisons tests were performed following one-way ANOVA for osmolarity experiment, and Student’s t test was performed for others: ns ≥ 0.05; *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001.

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    Figure 4.

    Proposed model and effect of osmolarity on body width. A, Schematic model depicting how Hydra changes body width depending on osmolarity. Light-blue arrows indicate the direction and speed of water accumulation, which swells Hydra’s body and activate mechanosensory system and contractions. B, Representative images showing width of Hydra’s body column at the end of elongation cycle, under control media (blue, above) or high-osmolarity solution (red, below). C, Representative traces showing changes in width over time under control media (blue) or high-osmolarity solution (red). D, Width of body column in control media (blue, 70.962 ± 6.560) or high-osmolarity solution (red, 46.540 ± 4.036). Line depicts the same animal in each condition. Error bars are shown as the mean ± SEM, with symbol marks denoting data points from individual Hydra (N = 4). Student’s t test was performed: *p < 0.05.

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    Table 1

    Statistical tests and results

    FigureDescriptionMethods95% CI of differenceSignificantp value
    1B Food: 0 vs 11–2.355 to 6.718No0.4707
    Food: 0 vs 41–3.537 to 5.537No0.8506
    Food: 1 vs 41–5.718 to 3.355No0.7981
    Osmo: Ctr vs low1–6.364 to 4.864No0.9432
    Osmo: Ctr vs high10.2450 to 10.25Yes0.038
    Osmo: Low vs high10.3148 to 11.69Yes0.0367
    Size: Ctr vs small2–9.991 to –2.937No0.0008
    Temp: Ctr vs high2–0.5233 to 6.023No0.0958
    1C Food: 0 vs 11–2.198 to 1.335No0.8207
    Food: 0 vs 41–1.448 to 2.085No0.898
    Food: 1 vs 41–0.9775 to 2.478No0.5411
    Osmo: Ctr vs low1–2.688 to 0.3822No0.1728
    Osmo: Ctr vs high11.034 to 3.682Yes0.0003
    Osmo: Low vs high11.958 to 5.064Yes<0.0001
    Size: Ctr vs small20.08979 to 2.894Yes0.0378
    Temp: Ctr vs high2–0.9724 to 1.722No0.5716
    1E Food: 0 vs 11–1.740 to 2.407No0.9195
    Food: 0 vs 410.3931 to 4.540Yes0.0164
    Food: 1 vs 410.05976 to 4.207Yes0.0426
    Osmo: Ctr vs low10.7542 to 6.579No0.01
    Osmo: Ctr vs high1–0.2806 to 4.642No0.0925
    Osmo: Low vs high1–3.947 to 0.9758Yes0.3223
    Size: Ctr vs small24.300 to 21.17No0.0059
    Temp: Ctr vs high2–6.122 to –2.412Yes<0.0001
    1F Food: 0 vs 11–1.026 to 0.09217No0.1178
    Food: 0 vs 41–1.426 to –0.3078Yes0.0014
    Food: 1 vs 41–0.9588 to 0.1588No0.2029
    Osmo: Ctr vs low11.610 to 3.724Yes<0.0001
    Osmo: Ctr vs high10.6877 to 2.474Yes0.0002
    Osmo: Low vs high1–1.979 to –0.1925Yes0.0134
    Size: Ctr vs small2–0.1413 to 0.9413No0.1413
    Temp: Ctr vs high2–2.683 to –0.9838Yes<0.0001
    2C Food: 0 vs 11–176.2 to 327.3No0.8033
    Food: 0 vs 41–257.1 to 281.1No0.9991
    Food: 1 vs 41–315.3 to 188.2No0.8705
    Osmo: Ctr vs low1–147.0 to 148.8No0.9998
    Osmo: Ctr vs high112.02 to 307.8Yes0.0356
    Osmo: Low vs high1–6.375 to 324.4No0.0588
    Size: Ctr vs small2–138.6 to 167.4No0.8303
    Temp: Ctr vs high2–132.3 to 152.1No0.8738
    2D Food: 0 vs 11–318.4 to 280.4No0.981
    Food: 0 vs 41–473.7 to 125.1No0.2655
    Food: 1 vs 41–475.4 to 164.8No0.378
    Osmo: Ctr vs low1–174.6 to 237.8No0.9107
    Osmo: Ctr vs high1–106.8 to 282.0No0.4681
    Osmo: Low vs high1–150.2 to 262.2No0.7494
    Size: Ctr vs small22.523 to 332.7Yes0.0473
    Temp: Ctr vs high2–20.35 to 199.1No0.0955
    2E Food: 0 vs 11–13.68 to 17.47No0.939
    Food: 0 vs 41–19.72 to 15.75No0.948
    Food: 1 vs 41–20.83 to 13.08No0.8034
    Osmo: Ctr vs low1–19.22 to 0.7527No0.0686
    Osmo: Ctr vs high1–6.431 to 13.54No0.5872
    Osmo: Low vs high11.625 to 23.96Yes0.0273
    Size: Ctr vs small2–7.207 to 13.24No0.5081
    Temp: Ctr vs high2–4.729 to 13.86No0.2836
    2F Food: 0 vs 11–19.97 to 13.83No0.9455
    Food: 0 vs 41–30.51 to 3.289No0.1296
    Food: 1 vs 41–28.61 to 7.526No0.3429
    Osmo: Ctr vs low1–18.81 to 7.069No0.4634
    Osmo: Ctr vs high1–7.909 to 16.49No0.6216
    Osmo: Low vs high1–2.777 to 23.11No0.1307
    Size: Ctr vs small22.745 to 22.78Yes0.0188
    Temp: Ctr vs high20.5891 to 18.07Yes0.0396
    2G Food: 0 vs 11–1.613 to 1.854No0.9773
    Food: 0 vs 41–0.8072 to 2.899No0.2839
    Food: 1 vs 41–0.8077 to 2.659No0.3176
    Osmo: Ctr vs low10.5862 to 3.721Yes0.0108
    Osmo: Ctr vs high11.379 to 4.514Yes0.0017
    Osmo: Low vs high1–0.9592 to 2.545No0.4373
    Size: Ctr vs small2–7.207 to 13.24No0.5081
    Temp: Ctr vs high2–4.729 to 13.86Yes0.2836
    2H Food: 0 vs 11–2.115 to 3.010No0.8669
    Food: 0 vs 41–2.517 to 2.607No0.9985
    Food: 1 vs 41–3.142 to 2.336No0.9032
    Osmo: Ctr vs low1–0.4909 to 5.189No0.1103
    Osmo: Ctr vs high1–2.518 to 2.609No0.9988
    Osmo: Low vs high1–5.037 to 0.4289No0.1028
    Size: Ctr vs small2–2.405 to 1.561No0.6416
    Temp: Ctr vs high2–2.067 to 1.073No0.4785
    3C Food: 0 vs 11–168.3 to 323.3No0.6736
    Food: 0 vs 41–276.1 to 190.3No0.8709
    Food: 1 vs 41–353.6 to 112.8No0.3699
    Osmo: Ctr vs low1–448.7 to –9.334Yes0.0406
    Osmo: Ctr vs high15.853 to 341.4Yes0.0422
    Osmo: Low vs high1192.3 to 612.9Yes0.0005
    Size: Ctr vs small2–96.12 to 287.7No0.288
    Temp: Ctr vs high2–173.1 to 196.4No0.8855
    3D Food: 0 vs 11–890.9 to 180.7No0.2575
    Food: 0 vs 41–594.9 to 429.8No0.9638
    Food: 1 vs 41–198.1 to 743.2No0.3624
    Osmo: Ctr vs low1–398.8 to 148.8No0.4752
    Osmo: Ctr vs high1–285.7 to 221.3No0.9411
    Osmo: Low vs high1–160.7 to 346.3No0.6139
    Size: Ctr vs small2–189.6 to 358.8No0.497
    Temp: Ctr vs high2–430.9 to 270.0No0.5946
    3E Food: 0 vs 11–20.65 to 14.51No0.8669
    Food: 0 vs 41–31.19 to 3.966No0.1246
    Food: 1 vs 41–29.33 to 8.249No0.2875
    Osmo: Ctr vs low1–18.11 to 16.66No0.9932
    Osmo: Ctr vs high1–9.921 to 18.47No0.7082
    Osmo: Low vs high1–12.39 to 22.38No0.7294
    Size: Ctr vs small2–4.836 to 10.90No0.406
    Temp: Ctr vs high2–4.654 to 17.22No0.2095
    3F Food: 0 vs 11–878.5 to 168.3No0.1957
    Food: 0 vs 41–583.0 to 417.9No0.8911
    Food: 1 vs 41–187.2 to 732.3No0.2734
    Osmo: Ctr vs low1–23.83 to 22.78No0.998
    Osmo: Ctr vs high1–25.81 to 12.84No0.6477
    Osmo: Low vs high1–28.53 to 16.61No0.7608
    Size: Ctr vs small2–6.952 to 12.37No0.536
    Temp: Ctr vs high2–4.654 to 17.22No0.2095
    3G Food: 0 vs 11–0.6621 to 3.852No0.1787
    Food: 0 vs 41–1.813 to 2.470No0.908
    Food: 1 vs 41–3.408 to 0.8747No0.2816
    Osmo: Ctr vs low1–6.687 to –1.087Yes0.0066
    Osmo: Ctr vs high1–0.5830 to 4.411No0.1499
    Osmo: Low vs high13.165 to 8.437Yes<0.0001
    Size: Ctr vs small2–1.356 to 3.915No0.3006
    Temp: Ctr vs high2–0.8085 to 4.736No0.1378
    3H Food: 0 vs 11–9.974 to 2.307No0.2484
    Food: 0 vs 41–6.661 to 4.990No0.919
    Food: 1 vs 41–2.828 to 8.823No0.3722
    Osmo: Ctr vs low1–389.9 to 139.9No0.4301
    Osmo: Ctr vs high1–382.1 to 229.7No0.7785
    Osmo: Low vs high1–257.1 to 354.7No0.901
    Size: Ctr vs small2–3.063 to 4.773No0.6283
    Temp: Ctr vs high2–6.933 to 3.432No0.4402
    4D High vs Ctr25.575 to 43.27Yes0.0193
    • Method 1 indicates ordinary one-way ANOVA, Tukey’s multiple comparison test, and method 2 indicates unpaired t test. The four conditions used were food (Food), osmolarity (Osmo), size (Size), and temperature (Temp). Control medium (ctr).

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  • Movie 1.

    Freely moving Hydra in control media. Animals were allowed to move freely in a Petri dish. Video was taken at 2 Hz and sped up 40-fold. Scale bar, 1 mm.

  • Movie 2.

    Ectoderm muscle activity in control media. The animal was allowed to move between coverslips in mounted configuration. Video was taken at 2 Hz and sped up 20-fold. Scale bar, 500 μm.

  • Movie 3.

    Neural activity in control media. The animal was allowed to move between coverslips in mounted configuration. Video was taken at 2 Hz and sped up 20-fold. Scale bar, 500 μm.

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Whole-Body Imaging of Neural and Muscle Activity during Behavior in Hydra vulgaris: Effect of Osmolarity on Contraction Bursts
Wataru Yamamoto, Rafael Yuste
eNeuro 22 July 2020, 7 (4) ENEURO.0539-19.2020; DOI: 10.1523/ENEURO.0539-19.2020

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Whole-Body Imaging of Neural and Muscle Activity during Behavior in Hydra vulgaris: Effect of Osmolarity on Contraction Bursts
Wataru Yamamoto, Rafael Yuste
eNeuro 22 July 2020, 7 (4) ENEURO.0539-19.2020; DOI: 10.1523/ENEURO.0539-19.2020
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