MDN brain descending neurons coordinately activate backward and inhibit forward locomotion
Command-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming (we define ‘command-like neuron’ as a neuron whose activation elicits or ‘commands’ a specific behavior). In most animals, it remains unknown how neural circuit...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2018-08-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/38554 |
| _version_ | 1797997591886036992 |
|---|---|
| author | Arnaldo Carreira-Rosario Aref Arzan Zarin Matthew Q Clark Laurina Manning Richard D Fetter Albert Cardona Chris Q Doe |
| author_facet | Arnaldo Carreira-Rosario Aref Arzan Zarin Matthew Q Clark Laurina Manning Richard D Fetter Albert Cardona Chris Q Doe |
| author_sort | Arnaldo Carreira-Rosario |
| collection | DOAJ |
| description | Command-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming (we define ‘command-like neuron’ as a neuron whose activation elicits or ‘commands’ a specific behavior). In most animals, it remains unknown how neural circuits switch between antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here, we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of Drosophila larval ‘mooncrawler descending neurons’ (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by stimulating a backward-active premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct monosynaptic reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals. |
| first_indexed | 2024-04-11T10:35:12Z |
| format | Article |
| id | doaj.art-f037d67d170a4ad28f2bc0f0943f2e3b |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:35:12Z |
| publishDate | 2018-08-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-f037d67d170a4ad28f2bc0f0943f2e3b2022-12-22T04:29:20ZengeLife Sciences Publications LtdeLife2050-084X2018-08-01710.7554/eLife.38554MDN brain descending neurons coordinately activate backward and inhibit forward locomotionArnaldo Carreira-Rosario0Aref Arzan Zarin1https://orcid.org/0000-0003-0484-3622Matthew Q Clark2https://orcid.org/0000-0002-1113-9388Laurina Manning3Richard D Fetter4https://orcid.org/0000-0002-1558-100XAlbert Cardona5https://orcid.org/0000-0003-4941-6536Chris Q Doe6https://orcid.org/0000-0001-5980-8029Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United StatesInstitute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United StatesInstitute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United StatesInstitute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesInstitute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United StatesCommand-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming (we define ‘command-like neuron’ as a neuron whose activation elicits or ‘commands’ a specific behavior). In most animals, it remains unknown how neural circuits switch between antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here, we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of Drosophila larval ‘mooncrawler descending neurons’ (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by stimulating a backward-active premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct monosynaptic reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals.https://elifesciences.org/articles/38554neural circuitlocomotorcommand neuronbehaviorbackward crawldescending neuron |
| spellingShingle | Arnaldo Carreira-Rosario Aref Arzan Zarin Matthew Q Clark Laurina Manning Richard D Fetter Albert Cardona Chris Q Doe MDN brain descending neurons coordinately activate backward and inhibit forward locomotion eLife neural circuit locomotor command neuron behavior backward crawl descending neuron |
| title | MDN brain descending neurons coordinately activate backward and inhibit forward locomotion |
| title_full | MDN brain descending neurons coordinately activate backward and inhibit forward locomotion |
| title_fullStr | MDN brain descending neurons coordinately activate backward and inhibit forward locomotion |
| title_full_unstemmed | MDN brain descending neurons coordinately activate backward and inhibit forward locomotion |
| title_short | MDN brain descending neurons coordinately activate backward and inhibit forward locomotion |
| title_sort | mdn brain descending neurons coordinately activate backward and inhibit forward locomotion |
| topic | neural circuit locomotor command neuron behavior backward crawl descending neuron |
| url | https://elifesciences.org/articles/38554 |
| work_keys_str_mv | AT arnaldocarreirarosario mdnbraindescendingneuronscoordinatelyactivatebackwardandinhibitforwardlocomotion AT arefarzanzarin mdnbraindescendingneuronscoordinatelyactivatebackwardandinhibitforwardlocomotion AT matthewqclark mdnbraindescendingneuronscoordinatelyactivatebackwardandinhibitforwardlocomotion AT laurinamanning mdnbraindescendingneuronscoordinatelyactivatebackwardandinhibitforwardlocomotion AT richarddfetter mdnbraindescendingneuronscoordinatelyactivatebackwardandinhibitforwardlocomotion AT albertcardona mdnbraindescendingneuronscoordinatelyactivatebackwardandinhibitforwardlocomotion AT chrisqdoe mdnbraindescendingneuronscoordinatelyactivatebackwardandinhibitforwardlocomotion |