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A circuit mechanism for the propagation of waves of muscle contraction in Drosophila.

Fushiki A, Zwart MF, Kohsaka H, Fetter RD, Cardona A, Nose A - Elife (2016)

Bottom Line: We found an intersegmental chain of synaptically connected neurons, alternating excitatory and inhibitory, necessary for wave propagation and active in phase with the wave.The inhibitory neurons (GDL) are necessary for both forward and backward locomotion, suggestive of different yet coupled central pattern generators, and its inhibition is necessary for wave propagation.The circuit structure and functional imaging indicated that the commands to contract one segment promote the relaxation of the next segment, revealing a mechanism for wave propagation in peristaltic locomotion.

View Article: PubMed Central - PubMed

Affiliation: Department of Complexity Science and Engineering, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan.

ABSTRACT
Animals move by adaptively coordinating the sequential activation of muscles. The circuit mechanisms underlying coordinated locomotion are poorly understood. Here, we report on a novel circuit for the propagation of waves of muscle contraction, using the peristaltic locomotion of Drosophila larvae as a model system. We found an intersegmental chain of synaptically connected neurons, alternating excitatory and inhibitory, necessary for wave propagation and active in phase with the wave. The excitatory neurons (A27h) are premotor and necessary only for forward locomotion, and are modulated by stretch receptors and descending inputs. The inhibitory neurons (GDL) are necessary for both forward and backward locomotion, suggestive of different yet coupled central pattern generators, and its inhibition is necessary for wave propagation. The circuit structure and functional imaging indicated that the commands to contract one segment promote the relaxation of the next segment, revealing a mechanism for wave propagation in peristaltic locomotion.

No MeSH data available.


Related in: MedlinePlus

Confirmation of the expression of ChR2 in GDLs.Expression of ChR2 reporters, ChR2(T159C)::YFP (A, B, C, E, F) driven by GDL-GAL4, and CsChrimson::mVenus driven by R15C11-LexA (D), in GDLs were confirmed. (A, B) tsh-GAL80 specifically eliminates GDL-GAL4-mediated expression in the VNC, without affecting the expression in cells in the brain, SEZ and the terminal (arrowheads). (C–F) Yellow and white arrows denote presynaptic terminals and cell bodies of GDLs, respectively. (A–D) Third instar, (E, F) First instar. (F) is a high magnification image of (E). Scale bar represents 80 μm in (A, B), 30 μm in (C, D), 20 μm in (E) and 10 μm in (F).DOI:http://dx.doi.org/10.7554/eLife.13253.022
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fig7s1: Confirmation of the expression of ChR2 in GDLs.Expression of ChR2 reporters, ChR2(T159C)::YFP (A, B, C, E, F) driven by GDL-GAL4, and CsChrimson::mVenus driven by R15C11-LexA (D), in GDLs were confirmed. (A, B) tsh-GAL80 specifically eliminates GDL-GAL4-mediated expression in the VNC, without affecting the expression in cells in the brain, SEZ and the terminal (arrowheads). (C–F) Yellow and white arrows denote presynaptic terminals and cell bodies of GDLs, respectively. (A–D) Third instar, (E, F) First instar. (F) is a high magnification image of (E). Scale bar represents 80 μm in (A, B), 30 μm in (C, D), 20 μm in (E) and 10 μm in (F).DOI:http://dx.doi.org/10.7554/eLife.13253.022

Mentions: The GDL-GAL4 (9-20-GAL4, iav-GAL80) drives expression in GDLs and a small number of cells in the brain and SEZ. All panels show dissected third instar larval CNS. (A–C) Morphology of GDLs was visualized with 10xUAS-IVS-myr::GFP reporter expressed by GDL-GAL4. Anti-GFP (green) and anti-FasII (magenta) antibodies were used. (A) A low magnification view showing GDL-GAL4 expression in a GDL (arrow) and in a small number of cells in the brain and SEZ (arrowheads). (B) A cross sectional view of an abdominal segment. White arrow denotes the cell body of a GDL in a dorsolateral area of the VNC. Yellow arrow denotes the presynaptic terminals of a GDL. (C) A dorsal view showing segmentally repeated GDLs in the VNC. Each GDL extends its neurites locally within the segment. Anterior is to the left and posterior is to the right. (D) An image of a fluorescently labelled single-cell clone of GDL (courtesy of James W. Truman, HHMI Janelia Research Campus). GDL is also annotated as A27j2. (E) UAS-syt::GFP was used as a reporter to visualize presynaptic terminals of GDLs (yellow arrows). Signals seen in a medial region (arrowhead) are likely presynaptic terminals of descending neurons from the brain or SEZ (Figure 7—figure supplement 1B). (F) The cell body of GDLs was positive for GABA. (G, H) Schematic drawings of GDLs. Scale bar represents 80 μm in (A), 30 μm in (C, E), 20 μm in (B), 10 μm in (D) and 5 μm in (F). (See also Figure 1—figure supplement 1.)


A circuit mechanism for the propagation of waves of muscle contraction in Drosophila.

Fushiki A, Zwart MF, Kohsaka H, Fetter RD, Cardona A, Nose A - Elife (2016)

Confirmation of the expression of ChR2 in GDLs.Expression of ChR2 reporters, ChR2(T159C)::YFP (A, B, C, E, F) driven by GDL-GAL4, and CsChrimson::mVenus driven by R15C11-LexA (D), in GDLs were confirmed. (A, B) tsh-GAL80 specifically eliminates GDL-GAL4-mediated expression in the VNC, without affecting the expression in cells in the brain, SEZ and the terminal (arrowheads). (C–F) Yellow and white arrows denote presynaptic terminals and cell bodies of GDLs, respectively. (A–D) Third instar, (E, F) First instar. (F) is a high magnification image of (E). Scale bar represents 80 μm in (A, B), 30 μm in (C, D), 20 μm in (E) and 10 μm in (F).DOI:http://dx.doi.org/10.7554/eLife.13253.022
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fig7s1: Confirmation of the expression of ChR2 in GDLs.Expression of ChR2 reporters, ChR2(T159C)::YFP (A, B, C, E, F) driven by GDL-GAL4, and CsChrimson::mVenus driven by R15C11-LexA (D), in GDLs were confirmed. (A, B) tsh-GAL80 specifically eliminates GDL-GAL4-mediated expression in the VNC, without affecting the expression in cells in the brain, SEZ and the terminal (arrowheads). (C–F) Yellow and white arrows denote presynaptic terminals and cell bodies of GDLs, respectively. (A–D) Third instar, (E, F) First instar. (F) is a high magnification image of (E). Scale bar represents 80 μm in (A, B), 30 μm in (C, D), 20 μm in (E) and 10 μm in (F).DOI:http://dx.doi.org/10.7554/eLife.13253.022
Mentions: The GDL-GAL4 (9-20-GAL4, iav-GAL80) drives expression in GDLs and a small number of cells in the brain and SEZ. All panels show dissected third instar larval CNS. (A–C) Morphology of GDLs was visualized with 10xUAS-IVS-myr::GFP reporter expressed by GDL-GAL4. Anti-GFP (green) and anti-FasII (magenta) antibodies were used. (A) A low magnification view showing GDL-GAL4 expression in a GDL (arrow) and in a small number of cells in the brain and SEZ (arrowheads). (B) A cross sectional view of an abdominal segment. White arrow denotes the cell body of a GDL in a dorsolateral area of the VNC. Yellow arrow denotes the presynaptic terminals of a GDL. (C) A dorsal view showing segmentally repeated GDLs in the VNC. Each GDL extends its neurites locally within the segment. Anterior is to the left and posterior is to the right. (D) An image of a fluorescently labelled single-cell clone of GDL (courtesy of James W. Truman, HHMI Janelia Research Campus). GDL is also annotated as A27j2. (E) UAS-syt::GFP was used as a reporter to visualize presynaptic terminals of GDLs (yellow arrows). Signals seen in a medial region (arrowhead) are likely presynaptic terminals of descending neurons from the brain or SEZ (Figure 7—figure supplement 1B). (F) The cell body of GDLs was positive for GABA. (G, H) Schematic drawings of GDLs. Scale bar represents 80 μm in (A), 30 μm in (C, E), 20 μm in (B), 10 μm in (D) and 5 μm in (F). (See also Figure 1—figure supplement 1.)

Bottom Line: We found an intersegmental chain of synaptically connected neurons, alternating excitatory and inhibitory, necessary for wave propagation and active in phase with the wave.The inhibitory neurons (GDL) are necessary for both forward and backward locomotion, suggestive of different yet coupled central pattern generators, and its inhibition is necessary for wave propagation.The circuit structure and functional imaging indicated that the commands to contract one segment promote the relaxation of the next segment, revealing a mechanism for wave propagation in peristaltic locomotion.

View Article: PubMed Central - PubMed

Affiliation: Department of Complexity Science and Engineering, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan.

ABSTRACT
Animals move by adaptively coordinating the sequential activation of muscles. The circuit mechanisms underlying coordinated locomotion are poorly understood. Here, we report on a novel circuit for the propagation of waves of muscle contraction, using the peristaltic locomotion of Drosophila larvae as a model system. We found an intersegmental chain of synaptically connected neurons, alternating excitatory and inhibitory, necessary for wave propagation and active in phase with the wave. The excitatory neurons (A27h) are premotor and necessary only for forward locomotion, and are modulated by stretch receptors and descending inputs. The inhibitory neurons (GDL) are necessary for both forward and backward locomotion, suggestive of different yet coupled central pattern generators, and its inhibition is necessary for wave propagation. The circuit structure and functional imaging indicated that the commands to contract one segment promote the relaxation of the next segment, revealing a mechanism for wave propagation in peristaltic locomotion.

No MeSH data available.


Related in: MedlinePlus