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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

Adjacency matrix for GDL circuits.Each row and column represents a neuron's’ pre- and post- synaptic contacts, respectively. The number in the matrix is the synapse number between the target neurons and their partners. Neurons are grouped by segments. GDLs are annotated as “A27j2_a1” in this figure.DOI:http://dx.doi.org/10.7554/eLife.13253.014
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fig4s3: Adjacency matrix for GDL circuits.Each row and column represents a neuron's’ pre- and post- synaptic contacts, respectively. The number in the matrix is the synapse number between the target neurons and their partners. Neurons are grouped by segments. GDLs are annotated as “A27j2_a1” in this figure.DOI:http://dx.doi.org/10.7554/eLife.13253.014

Mentions: Having identified GDLs as necessary for propagating peristaltic waves, we then studied the neural circuit basis for GDL function. First, we determined that GDLs do not synapse directly onto motor neurons by using GRASP (Feinberg et al., 2008; Gordon and Scott, 2009), expressing each half of the GFP protein in GDLs and motor neurons, respectively (Figure 4—figure supplement 1). To confirm this, we then identified GDLs in an electron microscopy (EM) volume comprising the entire larval CNS (Figure 4A) and reconstructed all neurons synaptically connected to GDLs in segment A1, none of which were motor neurons (Figure 4—figure supplement 2, 3). We also found that no strongly connected GDL partners synapse with each other, suggesting that GDLs act as hub neurons, with the potential to orchestrate activity patterns of postsynaptic neurons (Figure 4B). One of the top synaptic GDL partner cell types (by number of synapses), connected both presynaptically (“upstream”) and postsynaptically (“downstream”), is the segmentally repeated premotor interneuron A27h (Figure 4C,D and Figure 5—figure supplement 1A). Interestingly, though all the downstream premotor interneurons were found in the same segment as GDLs, all the upstream premotor interneurons were located in the next posterior segment (Figure 4D). Furthermore, GDLs receive the inputs from somatosensory neurons (vdaA and vdaC class II dendritic arborization neurons; Figure 4D) that likely mediate gentle touch (Tsubouchi et al., 2012). Taken together, this arrangement configures a feed-forward circuit in which premotor interneurons of one segment not only drive motor neurons in the same segment but also transmit an inhibitory signal to their own homologs in the adjacent anterior segment via GDLs (Figure 4E), in parallel with a synaptic pathway for sensory feedback that also regulates transmission of the peristaltic wave (see Discussion).10.7554/eLife.13253.011Figure 4.Circuit diagram around GDLs.


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)

Adjacency matrix for GDL circuits.Each row and column represents a neuron's’ pre- and post- synaptic contacts, respectively. The number in the matrix is the synapse number between the target neurons and their partners. Neurons are grouped by segments. GDLs are annotated as “A27j2_a1” in this figure.DOI:http://dx.doi.org/10.7554/eLife.13253.014
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Related In: Results  -  Collection

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fig4s3: Adjacency matrix for GDL circuits.Each row and column represents a neuron's’ pre- and post- synaptic contacts, respectively. The number in the matrix is the synapse number between the target neurons and their partners. Neurons are grouped by segments. GDLs are annotated as “A27j2_a1” in this figure.DOI:http://dx.doi.org/10.7554/eLife.13253.014
Mentions: Having identified GDLs as necessary for propagating peristaltic waves, we then studied the neural circuit basis for GDL function. First, we determined that GDLs do not synapse directly onto motor neurons by using GRASP (Feinberg et al., 2008; Gordon and Scott, 2009), expressing each half of the GFP protein in GDLs and motor neurons, respectively (Figure 4—figure supplement 1). To confirm this, we then identified GDLs in an electron microscopy (EM) volume comprising the entire larval CNS (Figure 4A) and reconstructed all neurons synaptically connected to GDLs in segment A1, none of which were motor neurons (Figure 4—figure supplement 2, 3). We also found that no strongly connected GDL partners synapse with each other, suggesting that GDLs act as hub neurons, with the potential to orchestrate activity patterns of postsynaptic neurons (Figure 4B). One of the top synaptic GDL partner cell types (by number of synapses), connected both presynaptically (“upstream”) and postsynaptically (“downstream”), is the segmentally repeated premotor interneuron A27h (Figure 4C,D and Figure 5—figure supplement 1A). Interestingly, though all the downstream premotor interneurons were found in the same segment as GDLs, all the upstream premotor interneurons were located in the next posterior segment (Figure 4D). Furthermore, GDLs receive the inputs from somatosensory neurons (vdaA and vdaC class II dendritic arborization neurons; Figure 4D) that likely mediate gentle touch (Tsubouchi et al., 2012). Taken together, this arrangement configures a feed-forward circuit in which premotor interneurons of one segment not only drive motor neurons in the same segment but also transmit an inhibitory signal to their own homologs in the adjacent anterior segment via GDLs (Figure 4E), in parallel with a synaptic pathway for sensory feedback that also regulates transmission of the peristaltic wave (see Discussion).10.7554/eLife.13253.011Figure 4.Circuit diagram around GDLs.

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