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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

A proposed circuit mechanism for moderating peristaltic locomotion.(A, B, D) EM reconstructions. (A) A candidate neuron for backward peristalsis. T01x3 is a homolog of A01x3 in thoracic segment. (B) A proprioceptive (vpda) and two other sensory neurons (vdaA and vdaC) synapse axo-dendritically onto A27h and axo-axonically onto a GDL of their own segment. (C) A proposed model of sensory feedback (per hemisegment). Note that the feedback have two simultaneous effects: promote the contraction of its own segment ahead of the wave, and then relaxation (or stretch) of the next anterior segment. (D) A descending neuron from the SEZ has connections with A27h neurons at each segment.DOI:http://dx.doi.org/10.7554/eLife.13253.026
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fig8s1: A proposed circuit mechanism for moderating peristaltic locomotion.(A, B, D) EM reconstructions. (A) A candidate neuron for backward peristalsis. T01x3 is a homolog of A01x3 in thoracic segment. (B) A proprioceptive (vpda) and two other sensory neurons (vdaA and vdaC) synapse axo-dendritically onto A27h and axo-axonically onto a GDL of their own segment. (C) A proposed model of sensory feedback (per hemisegment). Note that the feedback have two simultaneous effects: promote the contraction of its own segment ahead of the wave, and then relaxation (or stretch) of the next anterior segment. (D) A descending neuron from the SEZ has connections with A27h neurons at each segment.DOI:http://dx.doi.org/10.7554/eLife.13253.026

Mentions: The sequential intersegmental connections between the inhibitory GDL and the excitatory A27h neurons (Figure 4E) suggest that A27h may be active synchronously with the peristaltic wave of motor neuron activity that propagates locomotion. To test this hypothesis, we monitored the activity of A27h neurons and aCC motor neurons during fictive locomotion (Figure 6). We observed a wave-like activity that propagates from posterior to the anterior segments (Figure 6A). Interestingly, unlike GDLs that are active during both forward and backward locomotion (Video 5), A27h was activated only during forward locomotion (Figure 6B). This suggests that though GDL participates in both forward and backward locomotion, the excitatory neuron A27h is specialized in forward locomotion. We postulate a different premotor neuron acts during backward locomotion and we found a possible candidate for which a genetic driver line does not exist (Figure 8—figure supplement 1A and see Discussion).10.7554/eLife.13253.019Figure 6.A27h participates in forward motor activity.


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)

A proposed circuit mechanism for moderating peristaltic locomotion.(A, B, D) EM reconstructions. (A) A candidate neuron for backward peristalsis. T01x3 is a homolog of A01x3 in thoracic segment. (B) A proprioceptive (vpda) and two other sensory neurons (vdaA and vdaC) synapse axo-dendritically onto A27h and axo-axonically onto a GDL of their own segment. (C) A proposed model of sensory feedback (per hemisegment). Note that the feedback have two simultaneous effects: promote the contraction of its own segment ahead of the wave, and then relaxation (or stretch) of the next anterior segment. (D) A descending neuron from the SEZ has connections with A27h neurons at each segment.DOI:http://dx.doi.org/10.7554/eLife.13253.026
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Related In: Results  -  Collection

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fig8s1: A proposed circuit mechanism for moderating peristaltic locomotion.(A, B, D) EM reconstructions. (A) A candidate neuron for backward peristalsis. T01x3 is a homolog of A01x3 in thoracic segment. (B) A proprioceptive (vpda) and two other sensory neurons (vdaA and vdaC) synapse axo-dendritically onto A27h and axo-axonically onto a GDL of their own segment. (C) A proposed model of sensory feedback (per hemisegment). Note that the feedback have two simultaneous effects: promote the contraction of its own segment ahead of the wave, and then relaxation (or stretch) of the next anterior segment. (D) A descending neuron from the SEZ has connections with A27h neurons at each segment.DOI:http://dx.doi.org/10.7554/eLife.13253.026
Mentions: The sequential intersegmental connections between the inhibitory GDL and the excitatory A27h neurons (Figure 4E) suggest that A27h may be active synchronously with the peristaltic wave of motor neuron activity that propagates locomotion. To test this hypothesis, we monitored the activity of A27h neurons and aCC motor neurons during fictive locomotion (Figure 6). We observed a wave-like activity that propagates from posterior to the anterior segments (Figure 6A). Interestingly, unlike GDLs that are active during both forward and backward locomotion (Video 5), A27h was activated only during forward locomotion (Figure 6B). This suggests that though GDL participates in both forward and backward locomotion, the excitatory neuron A27h is specialized in forward locomotion. We postulate a different premotor neuron acts during backward locomotion and we found a possible candidate for which a genetic driver line does not exist (Figure 8—figure supplement 1A and see Discussion).10.7554/eLife.13253.019Figure 6.A27h participates in forward motor activity.

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