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Research ArticleNew Research, Sensory and Motor Systems

Influence of Temperature on Motor Behaviors in Newborn Opossums (Monodelphis domestica): An In Vitro Study

Edith Corriveau-Parenteau, Ariane Beauvais, Annie Angers and Jean-François Pflieger
eNeuro 16 May 2019, 6 (3) ENEURO.0347-18.2019; DOI: https://doi.org/10.1523/ENEURO.0347-18.2019
Edith Corriveau-Parenteau
Université de Montréal, Montréal, Quebec H3C 3J7, Canada
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Ariane Beauvais
Université de Montréal, Montréal, Quebec H3C 3J7, Canada
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Annie Angers
Université de Montréal, Montréal, Quebec H3C 3J7, Canada
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Jean-François Pflieger
Université de Montréal, Montréal, Quebec H3C 3J7, Canada
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  • Figure 1.
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    Figure 1.

    FL behavioral observation experiments. A, Schematic representation of the in vitro preparation. The specimen has skin over all its face, neck and FL, and the FL are free to move. 5G, trigeminal ganglion; Stim, stimulation. B, Serial photographs taken from video of either uncoordinated (upper rows) or rhythmic (left-right alternation; lower rows) responses after stimulation. Arrows indicate the direction of paw movements.

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    Figure 2.

    EMG experiments. A, Schematic representation of the preparations used in EMG recordings. FL were pinned on the bath floor (bath not illustrated) so as to limit movements. Skin was removed on the neck and FL, and EMG electrodes were implanted in triceps muscles. 5G, trigeminal ganglion; Stim, stimulation. B, Muscle activity following a stimulation. Bottom black trace, stimulation artifact produced by the pedal; red trace, raw recording from one EMG; blue trace, same trace as in red, but rectified and with a reduced sampling rate. The dashed lines delimitate the duration of the response used for analysis. C–E, Processed traces exemplifying reactions to stimulation of the left (L) and right (R) triceps muscles of the same animal: no-response (C), uncoordinated response (D), and rhythmic response (E). In B–E, the arrowheads indicate the beginning of the stimulation. The magenta lines in E are envelopes of burst responses highlighting the rhythmical alternation (not to scale with EMG traces).

  • Figure 3.
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    Figure 3.

    Percentage of FL responses of (A) 13 newborn opossums after cold (blue: 4°C, 21°C), neutral (orange: 25°C; bath temperature), or hot (red: 34°C) stimulations; (B) five of these specimens were tested for cold (4°C) both before and after trigeminal nerve transection (-5N) and, then, after spinal transection caudal to the obex (-obex). Each dot represents one specimen. Whisker plots stand for mean ± SEM, and thick horizontal lines indicate statistical differences between columns (Extended Data Fig. 3-1A,B); *p < 0.05, **p < 0.01, ****p < 0.0001.

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    Figure 4.

    Percentage of FL responses after cold (blue: 4°C), neutral (orange: 22°C; bath temperature) or hot (red: 45°C) stimulations (A) before and after transection of the spinal cord caudal to the obex (-obex) alone, or (B) after facial skin removal (-skin) followed by spinal transection. Each panel represents a series of experiments during which the specimens were consecutively stimulated. In both panels, each dot represents one specimen and whisker plots stand for mean ± SEM, and thick horizontal lines indicate statistical differences between columns (Extended Data Fig. 3-1C,D); *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001.

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    Figure 5.

    Response rates for all responses (“uncoordinated + rhythmic”; black columns) and rhythmic responses only (gray columns) after thermal stimulations (Stim T°) for all FL movements experiments (Extended Data Fig. 4-1). The neutral temperatures ([Bath T°]) are given for all cases. -5N, transection of the trigeminal nerve; -obex, transection of the neuraxis, caudally to the obex; -skin, removal of facial skin.

  • Figure 6.
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    Figure 6.

    EMG recordings of the triceps muscles following thermal stimulations. A, Response amplitudes to cold (blue: 4°C) or neutral (orange: 22°C; bath temperature), and hot (red: 45°C) temperatures before and after trigeminal nerve transection (-5N) and, then, after spinal transection caudal to the obex (-obex). The amplitude given represents the average of individual muscle responses that were normalized to the highest response amplitude for that muscle during the series of experiments. B, EMG amplitude of responses to cold, neutral, and hot temperature before (plain columns) and after (checkered columns) no-responses (amplitudes = 0) were removed from the analysis. In all panels, whisker plots stand for mean ± SEM, and thick horizontal lines indicate statistical differences between columns (Extended Data Fig. 5-1A,B); ***p < 0.001, ****p < 0.0001.

  • Figure 7.
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    Figure 7.

    Latencies of EMG responses after cold, neutral, and hot stimulations; each dot represents one triceps muscle response. In all panels, whisker plots stand for mean ± SEM, and thick horizontal lines indicate statistical differences between columns (Extended Data Fig. 6-1A); ****p < 0.0001.

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    Figure 8.

    TRPM8 immunoreactivity in transverse sections of cephalic tissues of newborn opossums. A–D, Trigeminal ganglia (approximately delineated by a dashed line) at P1 (A), P9 (B), and P13 (C, D) processed with (A–C) or without (D) the primary antibody against TRPM8. Labeled cell bodies are present only at P13 (examples pointed by arrowheads in C). The inset in C shows some labeled cell bodies at higher magnification. E, Labeled apical membrane of epithelial cells (empty arrowheads) in the trachea of a P9 opossum. F, Snout from a P9 opossum showing diffuse TRPM8 labeling in the epidermis (between empty arrowheads). Arrows in A, B, D–F point to blood vessels intrinsically fluorescent. Scale bar in F = 100 μm (for A–F).

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    Figure 9.

    RT-PCR gels of GAPDH and TRPM8 in the head of young opossums (P1, P12) and in the testes of an adult (T), illustrating the absence of TRPM8 mRNA expression at young ages.

Tables

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    Table 1.

    M. domestica specific primers used in RT-PCR experiments

    GeneSequence (5’-3’)
    GAPDHForward: TAAATGGGGAGATGCTGGAG
    Reverse: GCCAGCATCGAAGGTAGAAG
    TRPM8Forward: GGTCATTTGGGAGCAGACGA
    Reverse: ATCCATGAGCAGCACGTAGG
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    Table 2.

    Statistical tests performed for behavioral observations and EMG recordings

    FigureDescriptionData structureType of testp value
    A3AComparison between stimulations at cold (4°C), cool (21°C) neutral (25°C), hot (34°C)Paired, non-parametricKruskal–Wallis ANOVA<0.0001
    Cold vs coolDunn’s post hoc testn.s.
    Cold vs neutralDunn’s post hoc test<0.0001
    Cold vs hotDunn’s post hoc test<0.0001
    Cool vs neutralDunn’s post hoc test<0.01
    Cool vs hotDunn’s post hoc test<0.01
    Neutral vs hotDunn’s post hoc testn.s.
    B3BComparison between cold stimulations (4°C), cold -5N, and cold -obexPaired, non-parametricKruskal–Wallis ANOVA0.0411
    Cold vs cold -5NDunn’s post hoc testn.s.
    Cold vs cold -obexDunn’s post hoc test< 0.05.
    Cold -5N vs cold -obexDunn’s post hoc testn.s.
    C4AComparison between stimulations at cold (4°C), neutral (22°C), hot (45°C), and cold -obexPaired, non-parametricFriedman ANOVA<0.0001
    Cold vs neutralDunn’s post hoc test<0.001
    Cold vs hotDunn’s post hoc test<0.001
    Cold vs cold -obex Dunn’s post hoc testn.s.
    Neutral vs hotDunn’s post hoc testn.s.
    Neutral vs cold -obexDunn’s post hoc test<0.05
    Hot vs cold -obexDunn’s post hoc testn.s.
    DN/AComparison between responses in Figures 3, 4A when different temperatures are usedNon-parametric
    Neutral 22°C vs neutral 25°CKolmogorov–Smirnov t test0.2644
    Hot 34°C vs 45°CKolmogorov–Smirnov t test0.0495
    -obex with bath at 25°C vs 22°CKolmogorov–Smirnov t test<0.01
    EN/AComparison of response rates to cold (4°C) and neutral (22°C) following anesthesia by hypothermia or isofluraneNon-parametric
    Cold hypothermia vs isofluraneKolmogorov–Smirnov t test0.3077
    Neutral hypothermia vs isofluraneKolmogorov–Smirnov t test0.3874
    F4BComparison between stimulations at cold (4°C), neutral (22°C), hot (45°C), cold -skin, neutral -skin, hot -skin, and cold -obexPaired, non-parametricFriedman ANOVA<0.0001
    Cold vs neutralDunn’s post hoc test<0.01
    Cold vs hotDunn’s post hoc test<0.01
    Cold vs cold -skinDunn’s post hoc testn.s.
    Cold vs neutral -skinDunn’s post hoc test<0.0001
    Cold vs hot -skinDunn’s post hoc test<0.0001
    Cold vs cold -obexDunn’s post hoc test<0.001
    Neutral vs hotDunn’s post hoc testn.s.
    Neutral vs cold -skinDunn’s post hoc test<0.05
    Neutral vs neutral -skinDunn’s post hoc testn.s.
    Neutral vs hot -skinDunn’s post hoc testn.s.
    Neutral vs cold -obexDunn’s post hoc testn.s.
    Hot vs cold -skinDunn’s post hoc test<0.05
    Hot vs neutral -skinDunn’s post hoc testn.s.
    Hot vs hot -skinDunn’s post hoc testn.s.
    Hot vs cold -obexDunn’s post hoc testn.s.
    Cold -skin vs neutral -skinDunn’s post hoc test<0.0001
    Cold -skin vs hot -skinDunn’s post hoc test<0.001
    Cold -skin vs cold -obexDunn’s post hoc test<0.01
    Neutral -skin vs hot -skinDunn’s post hoc testn.s.
    Neutral -skin vs cold -obexDunn’s post hoc testn.s.
    Hot -skin vs cold -obexDunn’s post hoc testn.s.
    Cold vs cold-skinWilcoxon t test0.25
    Cold vs cold -obexWilcoxon t test0.0010
    Hot vs hot -skinWilcoxon t test0.0898
    Neutral vs neutral -skinWilcoxon t test0.0078
    Cold -skin vs cold-obexWilcoxon t test0.0015
    G6AEMG amplitudes for cold (4°C), neutral (22°C), hot (45°C) cold -5N, neutral -5N, hot -5N, and cold -obexUnpaired, non-parametricKruskal–Wallis ANOVA<0.0001
    Cold vs neutralDunn’s post hoc test<0.0001
    Cold vs hotDunn’s post hoc test<0.0001
    Cold vs cold -5NDunn’s post hoc test<0.0001
    Cold vs neutral -5NDunn’s post hoc test<0.0001
    Cold vs hot-5NDunn’s post hoc test<0.0001
    Cold vs cold -obexDunn’s post hoc test<0.0001
    Neutral vs hotDunn’s post hoc testn.s
    Neutral vs cold -5NDunn’s post hoc test<0.0001
    Neutral vs neutral -5NDunn’s post hoc test<0.01
    Neutral vs hot -5NDunn’s post hoc testn.s.
    Neutral vs cold -obexDunn’s post hoc testn.s.
    Hot vs cold -5NDunn’s post hoc test<0.001
    Hot vs neutral -5NDunn’s post hoc test<0.01
    Hot vs hot -5NDunn’s post hoc testn.s.
    Hot vs cold -obexDunn’s post hoc testn.s.
    Cold -5N vs neutral -5NDunn’s post hoc test<0.0001
    Cold -5N vs hot-5NDunn’s post hoc test<0.0001
    Cold -5N vs cold -obexDunn’s post hoc test<0.001
    Neutral -5N vs hot -5NDunn’s post hoc testn.s.
    Neutral -5N vs cold -obexDunn’s post hoc test<0.05
    Hot -5N vs cold -obexDunn’s post hoc testn.s.
    H6BEMG amplitudes comparisons for cold (4°C), neutral (22°C), hot (45°C) when all responses are considered and when only responses >0 are considered
    Cold vs cold >0Kolmogorov–Smirnov t test0.9998
    Neutral vs neutral >0Kolmogorov–Smirnov t test<0.0001
    Hot vs hot >0Kolmogorov–Smirnov t test<0.0001.
    I7Comparisons of latencies for cold (4°C), neutral (22°C), and hot (45°C)Unpaired, non-parametricKruskal–Wallis ANOVA<0.0001
    Cold vs neutralDunn’s post hoc test<0.0001
    Cold vs hotDunn’s post hoc test<0.0001
    Neutral vs hotDunn’s post hoc test<0.0001
    JN/AComparison of amplitudes after cold (4°C) stimulations for right and left FLUnpaired, non-parametricKolmogorov–Smirnov t test0.1726
    KN/AComparison of latencies after cold (4°C) stimulations for right and left FLUnpaired, non-parametricKolmogorov–Smirnov t test0.6001
    • -5N, trigeminal transection; -obex, complete transection of the spinoencephalic junction, caudal to the obex; -skin, facial skin removal; N/A, non-applicable; n.s., not significant.

Movies

  • Figures
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  • Extended Data
  • Movie 1.

    Ejection of liquid at bath temperature (22°C) toward the snout of an in vitro preparation of a P1 opossum do not induce motor response. The stimulation starts at the beginning of the video.

  • Movie 2.

    Uncoordinated response of the limbs induced by ejection of cold liquid (4°C) toward the snout of an in vitro preparation of a P1 opossum. The stimulation starts at the beginning of the video.

  • Movie 3.

    Rhythmic response of the limbs induced by ejection of cold liquid (4°C) toward the snout of an in vitro preparation of a P1 opossum. The stimulation starts at the beginning of the video.

Extended Data

  • Figures
  • Tables
  • Movies
  • Extended Data Figure 3-1

    FL response rates for behavioral observation experiments. Download Figure 3-1, DOCX file.

  • Extended Data Figure 4-1

    FL responses - either all responses (uncoordinated + rhythmic) or rhythmic responses only - induced by temperature in 34 in vitro preparations of newborn opossums in proportion of total stimulations. Download Figure 4-1, DOCX file.

  • Extended Data Figure 5-1

    Amplitude of EMG responses to different temperatures. Download Figure 5-1, DOCX file.

  • Extended Data Figure 6-1

    Latency of FL responses after temperature stimulations for EMG recordings. Download Figure 6-1, DOCX file.

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Influence of Temperature on Motor Behaviors in Newborn Opossums (Monodelphis domestica): An In Vitro Study
Edith Corriveau-Parenteau, Ariane Beauvais, Annie Angers, Jean-François Pflieger
eNeuro 16 May 2019, 6 (3) ENEURO.0347-18.2019; DOI: 10.1523/ENEURO.0347-18.2019

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Influence of Temperature on Motor Behaviors in Newborn Opossums (Monodelphis domestica): An In Vitro Study
Edith Corriveau-Parenteau, Ariane Beauvais, Annie Angers, Jean-François Pflieger
eNeuro 16 May 2019, 6 (3) ENEURO.0347-18.2019; DOI: 10.1523/ENEURO.0347-18.2019
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Keywords

  • development
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  • thermosensation
  • trigeminal system
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