Cargando…

A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila

Motor sequences are formed through the serial execution of different movements, but how nervous systems implement this process remains largely unknown. We determined the organizational principles governing how dirty fruit flies groom their bodies with sequential movements. Using genetically targeted...

Descripción completa

Detalles Bibliográficos
Autores principales: Seeds, Andrew M, Ravbar, Primoz, Chung, Phuong, Hampel, Stefanie, Midgley, Frank M, Mensh, Brett D, Simpson, Julie H
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4136539/
https://www.ncbi.nlm.nih.gov/pubmed/25139955
http://dx.doi.org/10.7554/eLife.02951
_version_ 1782331001862619136
author Seeds, Andrew M
Ravbar, Primoz
Chung, Phuong
Hampel, Stefanie
Midgley, Frank M
Mensh, Brett D
Simpson, Julie H
author_facet Seeds, Andrew M
Ravbar, Primoz
Chung, Phuong
Hampel, Stefanie
Midgley, Frank M
Mensh, Brett D
Simpson, Julie H
author_sort Seeds, Andrew M
collection PubMed
description Motor sequences are formed through the serial execution of different movements, but how nervous systems implement this process remains largely unknown. We determined the organizational principles governing how dirty fruit flies groom their bodies with sequential movements. Using genetically targeted activation of neural subsets, we drove distinct motor programs that clean individual body parts. This enabled competition experiments revealing that the motor programs are organized into a suppression hierarchy; motor programs that occur first suppress those that occur later. Cleaning one body part reduces the sensory drive to its motor program, which relieves suppression of the next movement, allowing the grooming sequence to progress down the hierarchy. A model featuring independently evoked cleaning movements activated in parallel, but selected serially through hierarchical suppression, was successful in reproducing the grooming sequence. This provides the first example of an innate motor sequence implemented by the prevailing model for generating human action sequences. DOI: http://dx.doi.org/10.7554/eLife.02951.001
format Online
Article
Text
id pubmed-4136539
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-41365392014-08-22 A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila Seeds, Andrew M Ravbar, Primoz Chung, Phuong Hampel, Stefanie Midgley, Frank M Mensh, Brett D Simpson, Julie H eLife Neuroscience Motor sequences are formed through the serial execution of different movements, but how nervous systems implement this process remains largely unknown. We determined the organizational principles governing how dirty fruit flies groom their bodies with sequential movements. Using genetically targeted activation of neural subsets, we drove distinct motor programs that clean individual body parts. This enabled competition experiments revealing that the motor programs are organized into a suppression hierarchy; motor programs that occur first suppress those that occur later. Cleaning one body part reduces the sensory drive to its motor program, which relieves suppression of the next movement, allowing the grooming sequence to progress down the hierarchy. A model featuring independently evoked cleaning movements activated in parallel, but selected serially through hierarchical suppression, was successful in reproducing the grooming sequence. This provides the first example of an innate motor sequence implemented by the prevailing model for generating human action sequences. DOI: http://dx.doi.org/10.7554/eLife.02951.001 eLife Sciences Publications, Ltd 2014-08-19 /pmc/articles/PMC4136539/ /pubmed/25139955 http://dx.doi.org/10.7554/eLife.02951 Text en Copyright © 2014, Seeds et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Seeds, Andrew M
Ravbar, Primoz
Chung, Phuong
Hampel, Stefanie
Midgley, Frank M
Mensh, Brett D
Simpson, Julie H
A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila
title A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila
title_full A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila
title_fullStr A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila
title_full_unstemmed A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila
title_short A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila
title_sort suppression hierarchy among competing motor programs drives sequential grooming in drosophila
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4136539/
https://www.ncbi.nlm.nih.gov/pubmed/25139955
http://dx.doi.org/10.7554/eLife.02951
work_keys_str_mv AT seedsandrewm asuppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT ravbarprimoz asuppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT chungphuong asuppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT hampelstefanie asuppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT midgleyfrankm asuppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT menshbrettd asuppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT simpsonjulieh asuppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT seedsandrewm suppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT ravbarprimoz suppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT chungphuong suppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT hampelstefanie suppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT midgleyfrankm suppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT menshbrettd suppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila
AT simpsonjulieh suppressionhierarchyamongcompetingmotorprogramsdrivessequentialgroomingindrosophila