A tale of two leeches: Toward the understanding of the evolution and development of behavioral neural circuits

Kuo, Dian‐Han; De‐Miguel, Francisco F.; Heath‐Heckman, Elizabeth A. C.; Szczupak, Lidia; Todd, Krista L.; Weisblat, David A.; Winchell, Christopher J.

doi:10.1111/ede.12358

Cited by 10 publications

(10 citation statements)

References 221 publications

(240 reference statements)

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“…Studies of different animal models have provided valuable insights on how motor circuits produce diverse motor outputs and how different muscles are coordinated during execution of a given motor behavior. In leech, some PMNs rhythmically oscillate in both swimming and crawling but with different frequencies; some fire in crawling but are silent in swimming [29]. In marine mollusk Tritonia Diomedea, the dorsal swim interneurons also make direct connections with the crawling-related cilia MNs and can induce crawling [30].…”

Section: Discussionmentioning

confidence: 99%

A premotor microcircuit to generate behavior-specific muscle activation patterns in Drosophila larvae

Huang

Zarin

2022

Preprint

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Animals can use a common set of muscles and motor neurons (MNs) to generate diverse locomotor behaviors, but how this is accomplished remains poorly understood. Previously, we characterized the muscle activity patterns for Drosophila larval forward and backward locomotion and found that ventral oblique (VO) muscles become active earlier in backward than in forward locomotion (Zarin et al. 2019). Here, we describe how premotor circuits generate differential activation timing of VO muscles. We identify inhibitory (A06c) and excitatory (A27h) premotor neurons (PMNs) with the greatest number of synapses with VO MNs. Strikingly, A06c is a bi-modal PMN that fires before and after VO MNs in forward locomotion but fires only after MNs in backward locomotion. Further, A27h is a forward-dedicated PMN active only in forward locomotion. These two PMNs interconnect with another forward-dedicated excitatory PMN (A18b3), to create feedforward inhibitory microcircuits that define the activity window for VO MNs/muscles, producing precise VO muscle patterns underlying forward locomotion. Silencing A06c, A27h or A18b3 PMN results in premature VO muscle activation in forward locomotion, resembling early VO activation in backward locomotion. Our results identify PMN micro-circuits that produce unique MN/muscle activity patterns to create behavior-specific motor output.

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Section: Discussionmentioning

confidence: 99%

A premotor microcircuit to generate behavior-specific muscle activation patterns in Drosophila larvae

Huang

Zarin

2022

Preprint

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“…Identifiable by electrical characteristics and function, each neuron plays a specific and unique role [ 12 ]. The differentiation of these nerve cells started at stage 6a in leech embryos [ 13 ], but the genes involved in the leech neural differentiation are not clear. Thus, elucidating the molecular mechanism of embryonic development in W. pigra could potentiate W. pigra as a model for developmental biology.…”

Section: Introductionmentioning

confidence: 99%

Division of developmental phases of freshwater leech Whitmania pigra and key genes related to neurogenesis revealed by whole genome and transcriptome analysis

Liu

et al. 2023

BMC Genomics

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The freshwater leech Whitmania pigra (W. pigra) Whitman (Annelida phylum) is a model organism for neurodevelopmental studies. However, molecular biology research on its embryonic development is still scarce. Here, we described a series of developmental stages of the W. pigra embryos and defined five broad stages of embryogenesis: cleavage stages, blastocyst stage, gastrula stage, organogenesis and refinement, juvenile. We obtained a total of 239.64 Gb transcriptome data of eight representative developmental phases of embryos (from blastocyst stage to maturity), which was then assembled into 21,482 unigenes according to our reference genome sequenced by single-molecule real-time (SMRT) long-read sequencing. We found 3114 genes differentially expressed during the eight phases with phase-specific expression pattern. Using a comprehensive transcriptome dataset, we demonstrated that 57, 49 and 77 DEGs were respectively related to morphogenesis, signal pathways and neurogenesis. 49 DEGs related to signal pathways included 30 wnt genes, 14 notch genes, and 5 hedgehog genes. In particular, we found a cluster consisting of 7 genes related to signal pathways as well as synapses, which were essential for regulating embryonic development. Eight genes cooperatively participated in regulating neurogenesis. Our results reveal the whole picture of W. pigra development mechanism from the perspective of transcriptome and provide new clues for organogenesis and neurodevelopmental studies of Annelida species.

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“…Identifiable by electrical characteristics and function, each neuron plays a specific and unique role (Nicholls and Baylor 1968). The differentiation of these nerve cells started at stage 6a in leech embryos (Kuo et al 2020), but the genes involved in the leech neural differentiation are not clear. Thus, elucidating the molecular mechanism of embryonic development has been a research hotspot in the scientific community.…”

Section: Introductionmentioning

confidence: 99%

Genome and transcriptome of freshwater leech Whitmania pigra reveal key genes related to morphogenesis, signal pathways and neurogenesis during embryonic development

Liu

et al. 2022

Preprint

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Whitmania pigra Whitman (phylum Annelida) is a widely distributed freshwater leech in East Asia, with an annual consumption of nearly 1,000 tons dry bodies for curing blood stasis syndrome. W. Pigra has be seen as a representative model organism of neurodevelopmental studies. Here, we sequenced a Chinese individual by sin-gle-molecule real-time (SMRT) long-read sequencing, and generated a de novo as-sembly of 178.87 Mb with contig N50 2.0 Mb. In addition, we obtained a total of 239.64 Gb transcriptome data of eight representative developmental phases of embryos (from blastocyst stage to maturity). Totally, 21482 genes were annotated, among these, 3114 genes were differentially expressed with phase-specific expression pattern, and mainly in the middle and late development (G, H, I, J phase). Using a comprehensive transcriptome dataset, we demonstrated that 57, 49 and 77 DEGs were respectively related to morphogenesis, signal pathways and neurogenesis. 49 DEGs related to signal pathways included 30 wnt genes, 14 notch genes, and 5 hedgehog genes. In par-ticular, we found a cluster consisting of 7 genes related to signal pathways as well as synapses, which were essential for regulating embryonic development. To some ex-tent, our results are helpful to reveal the whole picture of development mechanism from the perspective of transcriptome and also provide new clues for organogenesis and neurodevelopmental studies of Annelida species.

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A tale of two leeches: Toward the understanding of the evolution and development of behavioral neural circuits

Cited by 10 publications

References 221 publications

A premotor microcircuit to generate behavior-specific muscle activation patterns in Drosophila larvae

A premotor microcircuit to generate behavior-specific muscle activation patterns in Drosophila larvae

Division of developmental phases of freshwater leech Whitmania pigra and key genes related to neurogenesis revealed by whole genome and transcriptome analysis

Genome and transcriptome of freshwater leech Whitmania pigra reveal key genes related to morphogenesis, signal pathways and neurogenesis during embryonic development

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