Whole-body connectome of a segmented annelid larva
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eLife assessment
This study is an important advancement towards the understanding of animal nervous system organization and evolution by providing a compelling description of the entire connectome of the 3-day larva of the marine annelid Platynereis dumerilii. It provides a wealth of data on cell type diversity and the modules that interconnect them. Its strength in the massive amount of high-quality data is also partly a weakness as it can make it difficult to read and scientifically digest. This work lays the foundations for studies on cell type diversity, segmental vs. intersegmental connectivity, and mushroom bodies, but will certainly also be of use to scientists interested in other nervous systems parts, their functions, and evolution.
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Abstract
Nervous systems coordinate effectors across the body during movements. We know little about the cellular-level structure of synaptic circuits for such body-wide control. Here we describe the whole-body synaptic connectome of a segmented larva of the marine annelid Platynereis dumerilii . We reconstructed and annotated over 9,000 neuronal and non-neuronal cells in a whole-body serial electron microscopy dataset. Differentiated cells were classified into 202 neuronal and 92 non-neuronal cell types. We analyse modularity, multisensory integration, left-right and intersegmental connectivity and motor circuits for ciliated cells, glands, pigment cells and muscles. We identify several segment-specific cell types, demonstrating the heteromery of the annelid larval trunk. At the same time, segmentally repeated cell types across the head, the trunk segments and the pygidium suggest the serial homology of all segmental body regions. We also report descending and ascending pathways, peptidergic circuits and a multi-modal mechanosensory girdle. Our work provides the basis for understanding whole-body coordination in an entire segmented animal.
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eLife assessment
This study is an important advancement towards the understanding of animal nervous system organization and evolution by providing a compelling description of the entire connectome of the 3-day larva of the marine annelid Platynereis dumerilii. It provides a wealth of data on cell type diversity and the modules that interconnect them. Its strength in the massive amount of high-quality data is also partly a weakness as it can make it difficult to read and scientifically digest. This work lays the foundations for studies on cell type diversity, segmental vs. intersegmental connectivity, and mushroom bodies, but will certainly also be of use to scientists interested in other nervous systems parts, their functions, and evolution.
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Reviewer #1 (Public Review):
Summary:
This paper provides a resource for researchers studying the marine annelid Platynereis dumerilii. It is only the third whole-body connectome to be assembled and thus provides a comparison with those less complex animals: the nematode Caenorhabditis elegans and the tunicate Ciona intestinialis. The paper catalogs all cells in the body, not just neurons, and details how sensory neurons, interneurons, motor neurons, and effector organs are connected. From this, the authors are able to extract information about the organization of different aspects of the nervous system. These include the extent of recurrent connectivity, unimodal and multimodal sensory processing, and long-range and short-range connectivity.
Several interesting conclusions are drawn, including the concept that circuit evolution might …
Reviewer #1 (Public Review):
Summary:
This paper provides a resource for researchers studying the marine annelid Platynereis dumerilii. It is only the third whole-body connectome to be assembled and thus provides a comparison with those less complex animals: the nematode Caenorhabditis elegans and the tunicate Ciona intestinialis. The paper catalogs all cells in the body, not just neurons, and details how sensory neurons, interneurons, motor neurons, and effector organs are connected. From this, the authors are able to extract information about the organization of different aspects of the nervous system. These include the extent of recurrent connectivity, unimodal and multimodal sensory processing, and long-range and short-range connectivity.
Several interesting conclusions are drawn, including the concept that circuit evolution might have proceeded by duplication and diversion of cell types, much as it has been posited that gene evolution has occurred. It also informs the understanding of the evolution of segmental body plans in annelids by mapping and comparing cells in each segment.
Strengths:
This paper contains a wealth of data. The raw dataset is available. The codes and scripts are provided to allow interested readers to utilize this dataset.
The analysis is painstakingly meticulous. The diagrams are organized to orient the reader to the complexities of this overwhelming analysis
Weaknesses:
The strength of the paper is also its weakness. It contains so much data and analysis that it is burdensome to read and understand. There are 16 multi-panel data figures in the main text, and \another 38 supplemental figures, and 5 videos.
The impact of the paper is diminished by its size and depth. The paper could be broken up into smaller thematic papers that would be more accessible to researchers interested in particular topics. For example, there could be a single paper on the mushroom body and another paper on the segmental organization.
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Reviewer #2 (Public Review):
Summary:
The stated ambition of the authors in this manuscript is to thoroughly analyze the complete neural connectome of the three-day larva of the marine annelid Platynereis. This manuscript follows several previous publications by the same group on the same volume of serial EM data, addressing several specialized functional circuits, and supersedes a previous preprint published in 2020. To this end, the authors have annotated the whole cell complement of the larva, including non-neural cells, with the collaborative tool CATMAID, traced the whole neurite extensions of neural cells, and annotated all synapses. The connectome has been algorithmically analyzed to extract the principal modules, adding several new, so far unexplored neural circuits to the list.
Strengths:
This remarkable study adds a third …
Reviewer #2 (Public Review):
Summary:
The stated ambition of the authors in this manuscript is to thoroughly analyze the complete neural connectome of the three-day larva of the marine annelid Platynereis. This manuscript follows several previous publications by the same group on the same volume of serial EM data, addressing several specialized functional circuits, and supersedes a previous preprint published in 2020. To this end, the authors have annotated the whole cell complement of the larva, including non-neural cells, with the collaborative tool CATMAID, traced the whole neurite extensions of neural cells, and annotated all synapses. The connectome has been algorithmically analyzed to extract the principal modules, adding several new, so far unexplored neural circuits to the list.
Strengths:
This remarkable study adds a third species to the list of animals in which the full connectome and functional modules have been analyzed, alongside C. elegans and Ciona intestinalis. It represents a leap in phylogeny, with Platynereis being a representative of the lophotrochozoans. Also, Platynereis has considerably more neurons than the latter species. The study provides a complete picture of the set of neural modules that are necessary for the survival of an autonomous marine larva with an active lifestyle.
The analysis is particularly impressive for revealing the complete innervation of the entire set of effector cells in the Platynereis larva, including muscle fibers, glands, pigment cells, ciliated cells, and helping understand the overall control of the organism's behavior through multiple sensory pathway integrations. It also reveals layers of neuronal intercalation in sensory-effector pathways that allow further integration even in a larva with limited behavioral complexity. The structure of the developing mushroom bodies, proposed ancestral bilaterian brain sensory integrative units, is detailed, as well as a complex mechanosensory module specific to a swimming larva.
A key new aspect of this connectome study is the thorough analysis of segmental cell types and intersegmental connectivity. Metameric organization is widespread in bilaterians and is nowhere clearer than in annelids. This metameric organization is even proposed by some authors to be an ancestral trait of bilaterians. Here, the authors show that homologous cell types and connectivity are shared not only by all segments of the animal but also by its non-segmental terminal parts (anterior prostomium and posterior pygidium). They suggest, in turn, that the entire body of the annelid may be formed of ancestral metameric units, an idea proposed before but here strongly supported by a list of homologous cell types. This is the most thorough evidence obtained so far for this provocative and stimulating evolutionary hypothesis.
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