Extensive and diverse patterns of cell death sculpt neural networks in insects

Changes to the structure and function of neural networks are thought to underlie the evolutionary adaptation of animal behaviours. Among the many developmental phenomena that generate change programmed cell death (PCD) appears to play a key role. We show that cell death occurs continuously throughou...

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Main Authors: Sinziana Pop, Chin-Lin Chen, Connor J Sproston, Shu Kondo, Pavan Ramdya, Darren W Williams
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/59566
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author Sinziana Pop
Chin-Lin Chen
Connor J Sproston
Shu Kondo
Pavan Ramdya
Darren W Williams
author_facet Sinziana Pop
Chin-Lin Chen
Connor J Sproston
Shu Kondo
Pavan Ramdya
Darren W Williams
author_sort Sinziana Pop
collection DOAJ
description Changes to the structure and function of neural networks are thought to underlie the evolutionary adaptation of animal behaviours. Among the many developmental phenomena that generate change programmed cell death (PCD) appears to play a key role. We show that cell death occurs continuously throughout insect neurogenesis and happens soon after neurons are born. Mimicking an evolutionary role for increasing cell numbers, we artificially block PCD in the medial neuroblast lineage in Drosophila melanogaster, which results in the production of ‘undead’ neurons with complex arborisations and distinct neurotransmitter identities. Activation of these ‘undead’ neurons and recordings of neural activity in behaving animals demonstrate that they are functional. Focusing on two dipterans which have lost flight during evolution we reveal that reductions in populations of flight interneurons are likely caused by increased cell death during development. Our findings suggest that the evolutionary modulation of death-based patterning could generate novel network configurations.
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spelling doaj.art-dd411e8e76224131895babedf8d34be92022-12-22T03:52:56ZengeLife Sciences Publications LtdeLife2050-084X2020-09-01910.7554/eLife.59566Extensive and diverse patterns of cell death sculpt neural networks in insectsSinziana Pop0https://orcid.org/0000-0002-8811-8307Chin-Lin Chen1https://orcid.org/0000-0002-4968-4920Connor J Sproston2https://orcid.org/0000-0003-2491-0589Shu Kondo3https://orcid.org/0000-0002-4625-8379Pavan Ramdya4https://orcid.org/0000-0001-5425-4610Darren W Williams5https://orcid.org/0000-0001-5917-4935Centre for Developmental Neurobiology, King's College London, London, United KingdomNeuroengineering Laboratory, Brain Mind Institute and Institute of Bioengineering, École Polytechnique Fédérale de Lausanne, Lausanne, SwitzerlandCentre for Developmental Neurobiology, King's College London, London, United KingdomGenetic Strains Research Center, National Institute of Genetics, Shizuoka, JapanNeuroengineering Laboratory, Brain Mind Institute and Institute of Bioengineering, École Polytechnique Fédérale de Lausanne, Lausanne, SwitzerlandCentre for Developmental Neurobiology, King's College London, London, United KingdomChanges to the structure and function of neural networks are thought to underlie the evolutionary adaptation of animal behaviours. Among the many developmental phenomena that generate change programmed cell death (PCD) appears to play a key role. We show that cell death occurs continuously throughout insect neurogenesis and happens soon after neurons are born. Mimicking an evolutionary role for increasing cell numbers, we artificially block PCD in the medial neuroblast lineage in Drosophila melanogaster, which results in the production of ‘undead’ neurons with complex arborisations and distinct neurotransmitter identities. Activation of these ‘undead’ neurons and recordings of neural activity in behaving animals demonstrate that they are functional. Focusing on two dipterans which have lost flight during evolution we reveal that reductions in populations of flight interneurons are likely caused by increased cell death during development. Our findings suggest that the evolutionary modulation of death-based patterning could generate novel network configurations.https://elifesciences.org/articles/59566Braula coecaCrataerina pallidaThermobia domestica
spellingShingle Sinziana Pop
Chin-Lin Chen
Connor J Sproston
Shu Kondo
Pavan Ramdya
Darren W Williams
Extensive and diverse patterns of cell death sculpt neural networks in insects
eLife
Braula coeca
Crataerina pallida
Thermobia domestica
title Extensive and diverse patterns of cell death sculpt neural networks in insects
title_full Extensive and diverse patterns of cell death sculpt neural networks in insects
title_fullStr Extensive and diverse patterns of cell death sculpt neural networks in insects
title_full_unstemmed Extensive and diverse patterns of cell death sculpt neural networks in insects
title_short Extensive and diverse patterns of cell death sculpt neural networks in insects
title_sort extensive and diverse patterns of cell death sculpt neural networks in insects
topic Braula coeca
Crataerina pallida
Thermobia domestica
url https://elifesciences.org/articles/59566
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AT shukondo extensiveanddiversepatternsofcelldeathsculptneuralnetworksininsects
AT pavanramdya extensiveanddiversepatternsofcelldeathsculptneuralnetworksininsects
AT darrenwwilliams extensiveanddiversepatternsofcelldeathsculptneuralnetworksininsects