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Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex
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 tr...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Springer Berlin Heidelberg
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10354165/ https://www.ncbi.nlm.nih.gov/pubmed/36932234 http://dx.doi.org/10.1007/s00359-023-01616-y |
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author | Kandimalla, Pratyush Omoto, Jaison Jiro Hong, Elizabeth J. Hartenstein, Volker |
author_facet | Kandimalla, Pratyush Omoto, Jaison Jiro Hong, Elizabeth J. Hartenstein, Volker |
author_sort | Kandimalla, Pratyush |
collection | PubMed |
description | 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00359-023-01616-y. |
format | Online Article Text |
id | pubmed-10354165 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Springer Berlin Heidelberg |
record_format | MEDLINE/PubMed |
spelling | pubmed-103541652023-07-20 Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex Kandimalla, Pratyush Omoto, Jaison Jiro Hong, Elizabeth J. Hartenstein, Volker J Comp Physiol A Neuroethol Sens Neural Behav Physiol Review 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00359-023-01616-y. Springer Berlin Heidelberg 2023-03-17 2023 /pmc/articles/PMC10354165/ /pubmed/36932234 http://dx.doi.org/10.1007/s00359-023-01616-y Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Review Kandimalla, Pratyush Omoto, Jaison Jiro Hong, Elizabeth J. Hartenstein, Volker Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex |
title | Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex |
title_full | Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex |
title_fullStr | Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex |
title_full_unstemmed | Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex |
title_short | Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex |
title_sort | lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex |
topic | Review |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10354165/ https://www.ncbi.nlm.nih.gov/pubmed/36932234 http://dx.doi.org/10.1007/s00359-023-01616-y |
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