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

Autoři: John M. Barrett aff001;  Martinna G. Raineri Tapies aff001;  Gordon M. G. Shepherd aff001
Působiště autorů: Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, United States of America aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: 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.

Klíčová slova:

Animal anatomy – Animal behavior – Eyes – Mice – Nose – Squirrels – Thumbs – Wheat


1. Lungmus JK, Angielczyk KD. Antiquity of forelimb ecomorphological diversity in the mammalian stem lineage (Synapsida). Proc Natl Acad Sci U S A. 2019;116(14):6903–7. doi: 10.1073/pnas.1802543116 30886085; PubMed Central PMCID: PMC6452662.

2. Kardong KV. Vertebrates: Comparative Anatomy, Function, Evolution. 7 ed. New York: McGraw-Hill; 2015.

3. Phillips CG. Movements of the hand. Liverpool: Liverpool University Press; 1985.

4. Cheney PD, Fetz EE. Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol. 1980;44(4):773–91. doi: 10.1152/jn.1980.44.4.773 6253605.

5. Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M. Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res. 1988;71(3):491–507. doi: 10.1007/bf00248742 3416965.

6. Woolsey CN. Organization of somatic sensory and motor areas of the cerebral cortex. In: Harlow HF, Woolsey CN, editors. Biological and Biochemical Bases of Behaviour. Madison, Wisconsin: University of Wisconsin Press; 1958. p. 63–81.

7. Waters RS, Li CX, McCandlish CA. Relationship between the organization of the forepaw barrel subfield and the representation of the forepaw in layer IV of rat somatosensory cortex. Exp Brain Res. 1995;103(2):183–97. doi: 10.1007/bf00231705 7789426.

8. Klein A, Sacrey LA, Whishaw IQ, Dunnett SB. The use of rodent skilled reaching as a translational model for investigating brain damage and disease. Neurosci Biobehav Rev. 2012;36(3):1030–42. doi: 10.1016/j.neubiorev.2011.12.010 22227413.

9. Fleckman P, Jaeger K, Silva KA, Sundberg JP. Comparative anatomy of mouse and human nail units. Anat Rec (Hoboken). 2013;296(3):521–32. doi: 10.1002/ar.22660 23408541; PubMed Central PMCID: PMC3579226.

10. Whishaw IQ, Coles BL. Varieties of paw and digit movement during spontaneous food handling in rats: postures, bimanual coordination, preferences, and the effect of forelimb cortex lesions. Behav Brain Res. 1996;77(1–2):135–48. doi: 10.1016/0166-4328(95)00209-x 8762164.

11. Greene EC. Anatomy of the Rat. Philadelphia: The American Philsophical Society; 1935.

12. Whishaw IQ, Sarna JR, Pellis SM. Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behav Brain Res. 1998;96(1–2):79–91. doi: 10.1016/s0166-4328(97)00200-3 9821545.

13. Bab I, Hajbi-Yonissi C, Gabet Y, Müller R. Micro-Tomographic Atlas of the Mouse Skeleton. New York: Springer; 2007.

14. Tsugane M, Yasuda M. Dermatoglyphics on volar skin of mice: the normal pattern. The Anatomical record. 1995;242(2):225–32. doi: 10.1002/ar.1092420212 7668408.

15. Mathis MW, Mathis A, Uchida N. Somatosensory cortex plays an essential role in forelimb motor adaptation in mice. Neuron. 2017;93(6):1493–503. doi: 10.1016/j.neuron.2017.02.049 28334611; PubMed Central PMCID: PMC5491974.

16. Mathis A, Mamidanna P, Cury KM, Abe T, Murthy VN, Mathis MW, et al. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat Neurosci. 2018;21(9):1281–9. doi: 10.1038/s41593-018-0209-y 30127430.

17. Guo JZ, Graves AR, Guo WW, Zheng J, Lee A, Rodriguez-Gonzalez J, et al. Cortex commands the performance of skilled movement. eLife. 2015;4:e10774. doi: 10.7554/eLife.10774 26633811; PubMed Central PMCID: PMC4749564.

18. Datta SR, Anderson DJ, Branson K, Perona P, Leifer A. Computational Neuroethology: A Call to Action. Neuron. 2019;104(1):11–24. doi: 10.1016/j.neuron.2019.09.038 31600508.

19. Whishaw IQ, Karl JM. The evolution of the hand as a tool in feeding behavior: the multiple motor channel theory of hand use. In: Bels V, Whishaw IQ, editors. Feeding in Vertebrates. Switzerland: Springer; 2019. p. 159–86.

20. Ayling OG, Harrison TC, Boyd JD, Goroshkov A, Murphy TH. Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice. Nat Methods. 2009;6(3):219–24. doi: 10.1038/nmeth.1303 19219033.

21. Galiñanes GL, Bonardi C, Huber D. Directional Reaching for Water as a Cortex-Dependent Behavioral Framework for Mice. Cell reports. 2018;22(10):2767–83. doi: 10.1016/j.celrep.2018.02.042 29514103; PubMed Central PMCID: PMC5863030.

22. Sustaita D, Pouydebat E, Manzano A, Abdala V, Hertel F, Herrel A. Getting a grip on tetrapod grasping: form, function, and evolution. Biological reviews of the Cambridge Philosophical Society. 2013;88(2):380–405. doi: 10.1111/brv.12010 23286759.

23. Iwaniuk AN, Whishaw IQ. On the origin of skilled forelimb movements. Trends Neurosci. 2000;23(8):372–6. doi: 10.1016/s0166-2236(00)01618-0 10906801.

24. Whishaw IQ, Dringenberg HC, Pellis SM. Spontaneous forelimb grasping in free feeding by rats: motor cortex aids limb and digit positioning. Behav Brain Res. 1992;48(2):113–25. doi: 10.1016/s0166-4328(05)80147-0 1616602.

25. Whishaw IQ, Mirza Agha B, Kuntz JR, Qandeel, Faraji J, Mohajerani MH. Tongue protrusions modify the syntax of skilled reaching for food by the mouse: Evidence for flexibility in action selection and shared hand/mouth central modulation of action. Behav Brain Res. 2018;341:37–44. doi: 10.1016/j.bbr.2017.12.006 29229548.

26. Pellis SM, Pellis VC. Anatomy is important, but need not be destiny: novel uses of the thumb in aye-ayes compared to other lemurs. Behav Brain Res. 2012;231(2):378–85. doi: 10.1016/j.bbr.2011.08.046 21924295.

27. Hartstone-Rose A, Dickinson E, Boettcher ML, Herrel A. A primate with a Panda's thumb: The anatomy of the pseudothumb of Daubentonia madagascariensis. American journal of physical anthropology. 2019. doi: 10.1002/ajpa.23936 31633197.

28. Whishaw IQ, Faraji J, Kuntz JR, Mirza Agha B, Metz GAS, Mohajerani MH. The syntactic organization of pasta-eating and the structure of reach movements in the head-fixed mouse. Scientific reports. 2017;7(1):10987. doi: 10.1038/s41598-017-10796-y 28887566; PubMed Central PMCID: PMC5591288.

29. Tennant KA, Asay AL, Allred RP, Ozburn AR, Kleim JA, Jones TA. The vermicelli and capellini handling tests: simple quantitative measures of dexterous forepaw function in rats and mice. Journal of visualized experiments: JoVE. 2010;(41). doi: 10.3791/2076 20689506; PubMed Central PMCID: PMC3039868.

30. Igarashi M, Wickens J. Kinematic analysis of bimanual movements during food handling by head-fixed rats. J Neurophysiol. 2019;121(2):490–9. doi: 10.1152/jn.00295.2018 30403548.

31. Bollu TP, Whitehead SC, Kardon B, Redd J, Liu MH, Goldberg JH. Tongue Kinematics. Cortex-dependent corrections as the mouse tongue reaches for, and misses, targets. bioRxiv.

32. Uchida N, Kepecs A, Mainen ZF. Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making. Nat Rev Neurosci. 2006;7(6):485–91. doi: 10.1038/nrn1933 16715056.

33. Shusterman R, Smear MC, Koulakov AA, Rinberg D. Precise olfactory responses tile the sniff cycle. Nat Neurosci. 2011;14(8):1039–44. doi: 10.1038/nn.2877 21765422.

34. Whishaw IQ, Tomie JA. Olfaction directs skilled forelimb reaching in the rat. Behav Brain Res. 1989;32(1):11–21. doi: 10.1016/s0166-4328(89)80067-1 2930630.

35. Wiltschko AB, Johnson MJ, Iurilli G, Peterson RE, Katon JM, Pashkovski SL, et al. Mapping Sub-Second Structure in Mouse Behavior. Neuron. 2015;88(6):1121–35. doi: 10.1016/j.neuron.2015.11.031 26687221; PubMed Central PMCID: PMC4708087.

36. Addou T, Krouchev NI, Kalaska JF. Motor cortex single-neuron and population contributions to compensation for multiple dynamic force fields. J Neurophysiol. 2015;113(2):487–508. doi: 10.1152/jn.00094.2014 25339714.

37. Allred RP, Adkins DL, Woodlee MT, Husbands LC, Maldonado MA, Kane JR, et al. The vermicelli handling test: a simple quantitative measure of dexterous forepaw function in rats. J Neurosci Methods. 2008;170(2):229–44. doi: 10.1016/j.jneumeth.2008.01.015 18325597; PubMed Central PMCID: PMC2394277.

38. De Filippis B, Musto M, Altabella L, Romano E, Canese R, Laviola G. Deficient Purposeful Use of Forepaws in Female Mice Modelling Rett Syndrome. Neural plasticity. 2015;2015:326184. doi: 10.1155/2015/326184 26185689; PubMed Central PMCID: PMC4491574.

39. Guo ZV, Hires SA, Li N, O'Connor DH, Komiyama T, Ophir E, et al. Procedures for behavioral experiments in head-fixed mice. PLoS One. 2014;9(2):e88678. doi: 10.1371/journal.pone.0088678 24520413.

40. Ullman-Cullere MH, Foltz CJ. Body condition scoring: a rapid and accurate method for assessing health status in mice. Laboratory animal science. 1999;49(3):319–23. 10403450.

41. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5. doi: 10.1038/nmeth.2089 22930834.

42. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–82. doi: 10.1038/nmeth.2019 22743772; PubMed Central PMCID: PMC3855844.

43. Nath T, Mathis A, Chen AC, Patel A, Bethge M, Mathis MW. Using DeepLabCut for 3D markerless pose estimation across species and behaviors. BioRxiv. 2018;476531.

44. Zagouras A, Kazantzidis A, Nikitidou E, Argiriou AA. Determination of measuring sites for solar irradiance, based on cluster analysis of satellite-derived cloud estimations. Sol Energy. 2013;97:1–11. doi: 10.1016/j.solener.2013.08.005 WOS:000326851400001.

45. Pratt V. Direct least-squares fitting of algebraic surfaces. SIGGRAPH '87 Proceedings of the 14th annual conference on computer graphics and interactive techniques. New York, NY: ACM; 1987. p. 145–52.

46. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological). 1995;57(1):289–300.

Článek vyšel v časopise


2020 Číslo 1
Nejčtenější tento týden