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Published July 2023 | Published
Journal Article Open

Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex

  • 1. ROR icon California Institute of Technology

Abstract

The representation and integration of internal and external cues is crucial for any organism to execute appropriate behaviors. In insects, a highly conserved region of the brain, the central complex (CX), functions in the representation of spatial information and behavioral states, as well as the transformation of this information into desired navigational commands. How does this relatively invariant structure enable the incorporation of information from the diversity of anatomical, behavioral, and ecological niches occupied by insects? Here, we examine the input channels to the CX in the context of their development and evolution. Insect brains develop from ~ 100 neuroblasts per hemisphere that divide systematically to form "lineages" of sister neurons, that project to their target neuropils along anatomically characteristic tracts. Overlaying this developmental tract information onto the recently generated Drosophila "hemibrain" connectome and integrating this information with the anatomical and physiological recording of neurons in other species, we observe neuropil and lineage-specific innervation, connectivity, and activity profiles in CX input channels. We posit that the proliferative potential of neuroblasts and the lineage-based architecture of information channels enable the modification of neural networks across existing, novel, and deprecated modalities in a species-specific manner, thus forming the substrate for the evolution and diversification of insect navigational circuits.

Additional Information

© The Author(s) 2023. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. We would like to extend our gratitude to Jan Funke for assistance with neurotransmitter predictions from the hemibrain dataset. We would like to thank Amir H. Behbahani for his valuable insight into the analysis and feedback on the manuscript. We also thank Giovanni Frighetto, Hannah Haberkern, and Shivam Chitnis for helpful discussions and feedback on the manuscript. This work was supported by the National Institutes of Health grants 1U01MH109147 to EJH and 2R01NS054814 to VH. Additionally, PK was supported by the Tianqiao and Chrissy Chen Graduate Innovator Grant CHEN.SYS4.CGIACY22. Contributions. PK, JJO, and VH conceptualized the project. PK performed all the connectome analysis, with inputs from VH on identification and annotation of tracts. JJO generated the neuroblast lineage clones. PK and JJO performed comparative analysis across species. PK and VH generated figures and visualizations with inputs from JJO and EJH. PK wrote the original draft of the manuscript with inputs from VH and JJO. PK, JJO, VH, and EJH contributed to the editing and reviewing of the manuscript. VH and EJH supervised the project. EJH and VH acquired funding for this project. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

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Additional details

Created:
November 21, 2023
Modified:
January 9, 2024