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Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements

The small first digit (D1) of the mouse’s hand resembles a volar pad, but its thumb-like anatomy suggests ethological importance for manipulating small objects. To explore this possibility, we recorded high-speed close-up video of mice eating seeds and other food items. Analyses of ethograms and aut...

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Autores principales: Barrett, John M., Raineri Tapies, Martinna G., Shepherd, Gordon M. G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6961851/
https://www.ncbi.nlm.nih.gov/pubmed/31940368
http://dx.doi.org/10.1371/journal.pone.0226774
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author Barrett, John M.
Raineri Tapies, Martinna G.
Shepherd, Gordon M. G.
author_facet Barrett, John M.
Raineri Tapies, Martinna G.
Shepherd, Gordon M. G.
author_sort Barrett, John M.
collection PubMed
description The small first digit (D1) of the mouse’s hand resembles a volar pad, but its thumb-like anatomy suggests ethological importance for manipulating small objects. To explore this possibility, we recorded high-speed close-up video of mice eating seeds and other food items. Analyses of ethograms and automated tracking with DeepLabCut revealed multiple distinct microstructural features of food-handling. First, we found that mice indeed made extensive use of D1 for dexterous manipulations. In particular, mice used D1 to hold food with either of two grip types: a pincer-type grasp, or a “thumb-hold” grip, pressing with D1 from the side. Thumb-holding was preferentially used for handling smaller items, with the smallest items held between the two D1s alone. Second, we observed that mice cycled rapidly between two postural modes while feeding, with the hands positioned either at the mouth (oromanual phase) or resting below (holding phase). Third, we identified two highly stereotyped D1-related movements during feeding, including an extraordinarily fast (~20 ms) “regrip” maneuver, and a fast (~100 ms) “sniff” maneuver. Lastly, in addition to these characteristic simpler movements and postures, we also observed highly complex movements, including rapid D1-assisted rotations of food items and dexterous simultaneous double-gripping of two food fragments. Manipulation behaviors were generally conserved for different food types, and for head-fixed mice. Wild squirrels displayed a similar repertoire of D1-related movements. Our results define, for the mouse, a set of kinematic building-blocks of manual dexterity, and reveal an outsized role for D1 in these actions.
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spelling pubmed-69618512020-01-26 Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements Barrett, John M. Raineri Tapies, Martinna G. Shepherd, Gordon M. G. PLoS One Research Article The small first digit (D1) of the mouse’s hand resembles a volar pad, but its thumb-like anatomy suggests ethological importance for manipulating small objects. To explore this possibility, we recorded high-speed close-up video of mice eating seeds and other food items. Analyses of ethograms and automated tracking with DeepLabCut revealed multiple distinct microstructural features of food-handling. First, we found that mice indeed made extensive use of D1 for dexterous manipulations. In particular, mice used D1 to hold food with either of two grip types: a pincer-type grasp, or a “thumb-hold” grip, pressing with D1 from the side. Thumb-holding was preferentially used for handling smaller items, with the smallest items held between the two D1s alone. Second, we observed that mice cycled rapidly between two postural modes while feeding, with the hands positioned either at the mouth (oromanual phase) or resting below (holding phase). Third, we identified two highly stereotyped D1-related movements during feeding, including an extraordinarily fast (~20 ms) “regrip” maneuver, and a fast (~100 ms) “sniff” maneuver. Lastly, in addition to these characteristic simpler movements and postures, we also observed highly complex movements, including rapid D1-assisted rotations of food items and dexterous simultaneous double-gripping of two food fragments. Manipulation behaviors were generally conserved for different food types, and for head-fixed mice. Wild squirrels displayed a similar repertoire of D1-related movements. Our results define, for the mouse, a set of kinematic building-blocks of manual dexterity, and reveal an outsized role for D1 in these actions. Public Library of Science 2020-01-15 /pmc/articles/PMC6961851/ /pubmed/31940368 http://dx.doi.org/10.1371/journal.pone.0226774 Text en © 2020 Barrett et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Barrett, John M.
Raineri Tapies, Martinna G.
Shepherd, Gordon M. G.
Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements
title Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements
title_full Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements
title_fullStr Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements
title_full_unstemmed Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements
title_short Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements
title_sort manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6961851/
https://www.ncbi.nlm.nih.gov/pubmed/31940368
http://dx.doi.org/10.1371/journal.pone.0226774
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