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Cited by 60Zebrafish Biomedical Research ApplicationsNeuroscience and Neuropharmacology ResearchMotor Control and Adaptation

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Regulation of locomotor speed and selection of active sets of neurons by V1 neurons

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Kimura, Yukiko, Higashijima, Shin-ichi·2019·Nature Communications
DOI 10.1038/s41467-019-09871-xPMC PMC6531463
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Abstract

During fast movements in vertebrates, slow motor units are thought to be deactivated due to the mechanical demands of muscle contraction, but the associated neuronal mechanisms for this are unknown. Here, we perform functional analyses of spinal V1 neurons by selectively killing them in larval zebrafish, revealing two functions of V1 neurons. The first is the long-proposed role of V1 neurons: they play an important role in shortening the cycle period during swimming by providing in-phase inhibition. The second is that V1 neurons play an important role in the selection of active sets of neurons. We show that strong inhibitory inputs coming from V1 neurons play a crucial role in suppressing the activities of slow-type V2a and motor neurons, and, consequently, of slow muscles during fast swimming. Our results thus highlight the critical role of spinal inhibitory neurons for silencing slow-component neurons during fast movements.

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Figures

Fig. 1 Firing patterns of V1 neurons in larval zebrafish. a A side view of the compound transgenic fish of Tg[en1b:Gal4] and Tg[UAS:Kaede]. The dashed lines indicate boundaries of the spinal cord. Scale bar, 20 μm. b A schematic illustration of the simultaneous recordings of a V1 neuron (loose-patch) and ventral root (VR). Fictive swimming was elicited by applying brief electrical stimulation near the tail. c An example of the recordings from the fast-type V1 neurons. The blue arrowhead shows the time point of electrical stimulation. In the right panel, the region shadowed in blue in the left panel is enlarged. d An example of the recordings from the slow-type V1 neurons. e Histogram of spike timings of fast-type V1 neurons during fast (50–65 Hz) swim (1387 swimming cycles from 29 cells). f Histogram of spike timings of slow-type V1 neurons during slow (25–35 Hz) swim (5782 swimming cycles from 10 cells). g Schematic diagram of the Kaede photo-conversion experiment (top). The bottom two panels show the recordings from early-born V1 neurons (red Kaede [shown in magenta], left) and late-born V1 neurons (green Kaede, right). Scale bar, 10 μm. h Firing probability of early-born V1 neurons (left, n = 25) and late-born V1 neurons (right, n = 22) in each cycle during fast (>50 Hz) and slow (<40 Hz) swim. Each colored circle represents each recorded cell. i Classification of the recorded V1 neurons. Out of the 25 early-born V1 neurons, n = 23 for fast-type and n = 2 for hybrid-type. Out of the 22 late-born V1 neurons, n = 9 for fast-type, n = 10 for slow-type, and n = 3 for hybrid-type. If the value of the firing probability during fast swim was more than double that during slow swim, the cell was considered a fast-type (and vice versa). If the difference was within the doubled value, the cell was considered a hybrid-type
Fig. 1 Firing patterns of V1 neurons in larval zebrafish. a A side view of the compound transgenic fish of Tg[en1b:Gal4] and Tg[UAS:Kaede]. The dashed lines indicate boundaries of the spinal cord. Scale bar, 20 μm. b A schematic illustration of the simultaneous recordings of a V1 neuron (loose-patch) and ventral root (VR). Fictive swimming was elicited by applying brief electrical stimulation near the tail. c An example of the recordings from the fast-type V1 neurons. The blue arrowhead shows the time point of electrical stimulation. In the right panel, the region shadowed in blue in the left panel is enlarged. d An example of the recordings from the slow-type V1 neurons. e Histogram of spike timings of fast-type V1 neurons during fast (50–65 Hz) swim (1387 swimming cycles from 29 cells). f Histogram of spike timings of slow-type V1 neurons during slow (25–35 Hz) swim (5782 swimming cycles from 10 cells). g Schematic diagram of the Kaede photo-conversion experiment (top). The bottom two panels show the recordings from early-born V1 neurons (red Kaede [shown in magenta], left) and late-born V1 neurons (green Kaede, right). Scale bar, 10 μm. h Firing probability of early-born V1 neurons (left, n = 25) and late-born V1 neurons (right, n = 22) in each cycle during fast (>50 Hz) and slow (<40 Hz) swim. Each colored circle represents each recorded cell. i Classification of the recorded V1 neurons. Out of the 25 early-born V1 neurons, n = 23 for fast-type and n = 2 for hybrid-type. Out of the 22 late-born V1 neurons, n = 9 for fast-type, n = 10 for slow-type, and n = 3 for hybrid-type. If the value of the firing probability during fast swim was more than double that during slow swim, the cell was considered a fast-type (and vice versa). If the difference was within the doubled value, the cell was considered a hybrid-typeCC BY · PubMed Central
Fig. 2 V1 ablation reduced cycle frequency in swimming. a Fluorescent images (green channel) of Tg[en1b:GFP] and Tg[en1b:loxP-RFP-loxP-DTA] fish with (bottom panel) or without (top panel) Tg[hoxa4a/9a:Cre]. Green fluorescent protein (GFP) expression in the spinal V1 neurons (arrow) is absent in the presence of Cre (En1-DTA), with GFP expression in the brain (triangle) and slow muscle cells in the middle region of the body (arrowhead) being intact. Scale bar, 250 μm. b, c Ventral root recordings of fictive swimming elicited by electrical stimulations (ESs) in a control (b) and an En1-DTA fish (c). d Swimming frequency of control and En1-DTA fish during the initial phase of ES swim (swimming elicited by electrical stimulation). Control: 54.8 ± 5.7 Hz, number of fish = 73. En1-DTA: 28.0 ± 2.9 Hz, n = 57. **P < 0.01 (two-tailed t test, P = 6.4 × 10−62). e Swimming frequency of control and En1-DTA fish during Non-ES swim. Swim cycles with frequencies within 20–40 Hz were picked up and averaged. Control: 30.5 ± 2.3 Hz, n = 73. En1-DTA: 27.1 ± 2.2 Hz, n = 57. **P < 0.01 (two-tailed t test, P = 2.6 × 10−14). Data are mean ± s.d.
Fig. 2 V1 ablation reduced cycle frequency in swimming. a Fluorescent images (green channel) of Tg[en1b:GFP] and Tg[en1b:loxP-RFP-loxP-DTA] fish with (bottom panel) or without (top panel) Tg[hoxa4a/9a:Cre]. Green fluorescent protein (GFP) expression in the spinal V1 neurons (arrow) is absent in the presence of Cre (En1-DTA), with GFP expression in the brain (triangle) and slow muscle cells in the middle region of the body (arrowhead) being intact. Scale bar, 250 μm. b, c Ventral root recordings of fictive swimming elicited by electrical stimulations (ESs) in a control (b) and an En1-DTA fish (c). d Swimming frequency of control and En1-DTA fish during the initial phase of ES swim (swimming elicited by electrical stimulation). Control: 54.8 ± 5.7 Hz, number of fish = 73. En1-DTA: 28.0 ± 2.9 Hz, n = 57. **P < 0.01 (two-tailed t test, P = 6.4 × 10−62). e Swimming frequency of control and En1-DTA fish during Non-ES swim. Swim cycles with frequencies within 20–40 Hz were picked up and averaged. Control: 30.5 ± 2.3 Hz, n = 73. En1-DTA: 27.1 ± 2.2 Hz, n = 57. **P < 0.01 (two-tailed t test, P = 2.6 × 10−14). Data are mean ± s.d.CC BY · PubMed Central
Fig. 3 Activity of motoneurons (MNs) in control and En1-DTA fish during fictive swimming. a Typical morphology of fast-type MNs. The horizontal dotted line at the top indicates the dorsal boundary of the trunk muscles. The horizontal dotted line at the bottom indicates the boundary of the dorsally located muscles and ventrally located muscles. Scale bar, 20 μm. b Typical morphology of slow-type MNs. Scale bar, 20 μm. c Example of simultaneous recordings between fast-type MNs (loose-patch) and ventral root (VR) in control fish. d Example of simultaneous recordings between fast-type MNs and VR in En1-DTA fish. e Example of simultaneous recordings between slow-type MNs and VR in control fish. f Example of simultaneous recordings between slow-type MNs and VR in En1-DTA fish. g, h Numbers of spikes (g) and firing probability in each cycle (h) during fast/strong swim. Each circle represents each cell (n = 8 for fast-type MNs in control [n = 6 for PMNs, n = 2 for dvs]; n = 14 for fast-type MNs in En1-DTA [n = 8 for PMNs, n = 6 for dvs]; n = 11 for slow-type MNs in control; n = 14 for slow-type MNs in En1-DTA). **P < 0.01 (Mann–Whitney U test, P = 0.14 [g, fast-type MNs], P = 3.5 × 10−5 [g, slow-type MNs], P = 0.11 [h, fast-type MNs] for fast-type MNs, P = 1.2 × 10−5 [h, slow-type MNs]). ns, not significant. Boxes represent the interquartile range (IQR) between first and third quartiles and the line inside represents the median. Whiskers denote the lowest and highest values within 1.5 × IQR from the first and third quartiles, respectively
Fig. 3 Activity of motoneurons (MNs) in control and En1-DTA fish during fictive swimming. a Typical morphology of fast-type MNs. The horizontal dotted line at the top indicates the dorsal boundary of the trunk muscles. The horizontal dotted line at the bottom indicates the boundary of the dorsally located muscles and ventrally located muscles. Scale bar, 20 μm. b Typical morphology of slow-type MNs. Scale bar, 20 μm. c Example of simultaneous recordings between fast-type MNs (loose-patch) and ventral root (VR) in control fish. d Example of simultaneous recordings between fast-type MNs and VR in En1-DTA fish. e Example of simultaneous recordings between slow-type MNs and VR in control fish. f Example of simultaneous recordings between slow-type MNs and VR in En1-DTA fish. g, h Numbers of spikes (g) and firing probability in each cycle (h) during fast/strong swim. Each circle represents each cell (n = 8 for fast-type MNs in control [n = 6 for PMNs, n = 2 for dvs]; n = 14 for fast-type MNs in En1-DTA [n = 8 for PMNs, n = 6 for dvs]; n = 11 for slow-type MNs in control; n = 14 for slow-type MNs in En1-DTA). **P < 0.01 (Mann–Whitney U test, P = 0.14 [g, fast-type MNs], P = 3.5 × 10−5 [g, slow-type MNs], P = 0.11 [h, fast-type MNs] for fast-type MNs, P = 1.2 × 10−5 [h, slow-type MNs]). ns, not significant. Boxes represent the interquartile range (IQR) between first and third quartiles and the line inside represents the median. Whiskers denote the lowest and highest values within 1.5 × IQR from the first and third quartiles, respectivelyCC BY · PubMed Central
Fig. 4 Voltage-clamp recordings from slow-type motoneurons (MNs) in control and En1-DTA fish. a Example of simultaneous recordings between slow-type MNs (voltage-clamp) and ventral root (VR) in control fish. The cell was held at −75 mV to reveal excitatory currents. b Example of simultaneous recordings between slow-type MNs and VR in control fish. The cell was held at +10 mV to reveal inhibitory currents. The right two panels show the enlargements of the regions shaded in blue. “In” represents the in-phase period (from −0.15 to +0.15 in the cycle, pink). “Anti” represents the anti-phase period (from 0.35 to 0.65, gray). c Example of simultaneous recordings between slow-type MNs and VR in En1-DTA fish. The cell was held at −75 mV to reveal excitatory currents. d Example of simultaneous recordings between slow-type MNs and VR in En1-DTA fish. The cell was held at +10 mV to reveal inhibitory currents. e Phase analysis of excitatory and inhibitory currents during fast/strong swim. Normalized currents (±s.e.m.) are shown. Top panel, control fish; bottom panel, En1-DTA. f, g Peak inhibitory (f) and excitatory (g) currents during fast/strong swim in control (left, n = 10) and En1-DTA (right, n = 11) fish. “In” represents the in-phase period. “Anti” represents the anti-phase period. Each circle represents each cell. **P < 0.01; *P < 0.05 (comparison between control and En1-DTA, Mann–Whitney U test, P = 0.0080 [f], P = 0.013 [g]; comparison between in-phase and anti-phase, Wilcoxon signed-rank test, P = 0.0020 [f, control], P = 0.0029 [f, En1-DTA], P = 0.0020 [g, control], P = 0.00098 [g, En1-DTA])
Fig. 4 Voltage-clamp recordings from slow-type motoneurons (MNs) in control and En1-DTA fish. a Example of simultaneous recordings between slow-type MNs (voltage-clamp) and ventral root (VR) in control fish. The cell was held at −75 mV to reveal excitatory currents. b Example of simultaneous recordings between slow-type MNs and VR in control fish. The cell was held at +10 mV to reveal inhibitory currents. The right two panels show the enlargements of the regions shaded in blue. “In” represents the in-phase period (from −0.15 to +0.15 in the cycle, pink). “Anti” represents the anti-phase period (from 0.35 to 0.65, gray). c Example of simultaneous recordings between slow-type MNs and VR in En1-DTA fish. The cell was held at −75 mV to reveal excitatory currents. d Example of simultaneous recordings between slow-type MNs and VR in En1-DTA fish. The cell was held at +10 mV to reveal inhibitory currents. e Phase analysis of excitatory and inhibitory currents during fast/strong swim. Normalized currents (±s.e.m.) are shown. Top panel, control fish; bottom panel, En1-DTA. f, g Peak inhibitory (f) and excitatory (g) currents during fast/strong swim in control (left, n = 10) and En1-DTA (right, n = 11) fish. “In” represents the in-phase period. “Anti” represents the anti-phase period. Each circle represents each cell. **P < 0.01; *P < 0.05 (comparison between control and En1-DTA, Mann–Whitney U test, P = 0.0080 [f], P = 0.013 [g]; comparison between in-phase and anti-phase, Wilcoxon signed-rank test, P = 0.0020 [f, control], P = 0.0029 [f, En1-DTA], P = 0.0020 [g, control], P = 0.00098 [g, En1-DTA])CC BY · PubMed Central
Fig. 5 Activity of ventrally located V2a neurons in control and En1-DTA fish. a Lateral view of the spinal cord of Tg[chx10:GFP]. The horizontal dashed lines indicate the dorsal and ventral boundaries of the spinal cord. Ventrally located V2a neurons (the position from 0 to 0.5) are the subjects of the recordings (top panel). The bottom two panels show the images of a loose-patch recording. Scale bar, 20 μm. b An example of simultaneous recordings between ventrally located V2a neurons (loose-patch) and ventral root (VR) in control fish. c An example of simultaneous recordings between ventrally located V2a neurons (loose-patch) and VR in En1-DTA fish. d, e Numbers of spikes (d) and firing probability in each cycle (e) during fast/strong swim. Each circle represents each cell (n = 84 for ventrally located V2a neurons in control; n = 60 for ventrally located V2a neurons in En1-DTA). **P < 0.01 (Mann–Whitney U test, P = 1.3 × 10−10 [d], P = 3.7 × 10−14 [e]). Boxes represent the interquartile range (IQR) between first and third quartiles and the line inside represents the median. Whiskers denote the lowest and highest values within 1.5 × IQR from the first and third quartiles, respectively
Fig. 5 Activity of ventrally located V2a neurons in control and En1-DTA fish. a Lateral view of the spinal cord of Tg[chx10:GFP]. The horizontal dashed lines indicate the dorsal and ventral boundaries of the spinal cord. Ventrally located V2a neurons (the position from 0 to 0.5) are the subjects of the recordings (top panel). The bottom two panels show the images of a loose-patch recording. Scale bar, 20 μm. b An example of simultaneous recordings between ventrally located V2a neurons (loose-patch) and ventral root (VR) in control fish. c An example of simultaneous recordings between ventrally located V2a neurons (loose-patch) and VR in En1-DTA fish. d, e Numbers of spikes (d) and firing probability in each cycle (e) during fast/strong swim. Each circle represents each cell (n = 84 for ventrally located V2a neurons in control; n = 60 for ventrally located V2a neurons in En1-DTA). **P < 0.01 (Mann–Whitney U test, P = 1.3 × 10−10 [d], P = 3.7 × 10−14 [e]). Boxes represent the interquartile range (IQR) between first and third quartiles and the line inside represents the median. Whiskers denote the lowest and highest values within 1.5 × IQR from the first and third quartiles, respectivelyCC BY · PubMed Central
Fig. 6 Voltage-clamp recordings of fast and slow muscles in control and En1-DTA fish. a A schematic illustration of the simultaneous voltage-clamp recordings of two muscle cells (one for a fast muscle, the other for a slow muscle). Neuro-muscular transmission was partially blocked in these experiments, and portions of synaptic currents remained in the recording conditions. b An image after a recording. Slow and fast muscles were morphologically distinct and could be easily distinguished. Scale bar, 20 μm. c Example of simultaneous voltage-clamp recordings in control fish. d Example of simultaneous voltage-clamp recordings in En1-DTA fish. e Normalized currents in the slow muscle cells in the cycle when the fast muscle received strong inputs (>50% of the maximum). Five paired recordings were performed. Control: 0.44 ± 0.08, En1-DTA: 0.73 ± 0.04. Data are mean ± s.d. **P < 0.01 (two-tailed t test, P = 0.00091)
Fig. 6 Voltage-clamp recordings of fast and slow muscles in control and En1-DTA fish. a A schematic illustration of the simultaneous voltage-clamp recordings of two muscle cells (one for a fast muscle, the other for a slow muscle). Neuro-muscular transmission was partially blocked in these experiments, and portions of synaptic currents remained in the recording conditions. b An image after a recording. Slow and fast muscles were morphologically distinct and could be easily distinguished. Scale bar, 20 μm. c Example of simultaneous voltage-clamp recordings in control fish. d Example of simultaneous voltage-clamp recordings in En1-DTA fish. e Normalized currents in the slow muscle cells in the cycle when the fast muscle received strong inputs (>50% of the maximum). Five paired recordings were performed. Control: 0.44 ± 0.08, En1-DTA: 0.73 ± 0.04. Data are mean ± s.d. **P < 0.01 (two-tailed t test, P = 0.00091)CC BY · PubMed Central
Fig. 7 Proposed model of the functions of V1 neurons. a During fast swimming, excitatory neurons (pink) provide strong phasic excitation to fast-swimming circuits (thick pink line). Excitatory neurons (pink) also provide moderate phasic excitation to fast-swimming circuits (thin pink line). Fast-type V1 neurons provide strong phasic inhibition to both of the circuits (thick blue lines). The strong phasic inhibition of fast-swimming circuits plays a role in frequency regulation. The strong phasic inhibition of slow-swimming circuits plays a role in shutting down the activities of the component neurons. b During slow swimming, excitatory neurons (pink) provide phasic excitation to slow-swimming circuits (pink line). Slow-type V1 neurons provide phasic inhibition to the circuit (blue line). The phasic inhibition plays a role in frequency regulation
Fig. 7 Proposed model of the functions of V1 neurons. a During fast swimming, excitatory neurons (pink) provide strong phasic excitation to fast-swimming circuits (thick pink line). Excitatory neurons (pink) also provide moderate phasic excitation to fast-swimming circuits (thin pink line). Fast-type V1 neurons provide strong phasic inhibition to both of the circuits (thick blue lines). The strong phasic inhibition of fast-swimming circuits plays a role in frequency regulation. The strong phasic inhibition of slow-swimming circuits plays a role in shutting down the activities of the component neurons. b During slow swimming, excitatory neurons (pink) provide phasic excitation to slow-swimming circuits (pink line). Slow-type V1 neurons provide phasic inhibition to the circuit (blue line). The phasic inhibition plays a role in frequency regulationCC BY · PubMed Central

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Authors
Kimura, Y., & Higashijima, S.-I.
Affiliations
National Institute for Basic Biology (JP)
Corresponding author
Higashijima, Shin-ichi
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2019-05-22
Volume
10
Issue
1
Pages
2268-2268
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-019-09871-x
PMC
PMC6531463
OpenAlex
W2945632060
Cited by
60
References
8
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Type
journal article
Language
en
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Locations
  • Nature Communications (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Ministry of Education, Culture, Sports, Science and Technology
  • Japan Society for the Promotion of Science (16K07022, 19K06897)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Keywords
V1 neurons, swimming, slow motor units, neuronal silencing, zebrafish larvae, motor neuron inhibition
MeSH terms
Animals, Anterior Horn Cells, Embryo, Nonmammalian, Larva, Swimming, Zebrafish, Models, Animal, Animals, Genetically Modified, Renshaw Cells

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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