Manipulation-specific cortical activity as mice handle food.
electrophysiology
food handling
forelimb
generalized linear model
manual dexterity
motor cortex
non-negative matrix factorization
optogenetics
oromanual
somatosensory cortex
Journal
Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782
Informations de publication
Date de publication:
21 11 2022
21 11 2022
Historique:
received:
27
05
2022
revised:
02
09
2022
accepted:
22
09
2022
pubmed:
16
10
2022
medline:
25
11
2022
entrez:
15
10
2022
Statut:
ppublish
Résumé
Food handling offers unique yet largely unexplored opportunities to investigate how cortical activity relates to forelimb movements in a natural, ethologically essential, and kinematically rich form of manual dexterity. To determine these relationships, we recorded high-speed (1,000 fps) video and multi-channel electrophysiological cortical spiking activity while mice handled food. The high temporal resolution of the video allowed us to decompose active manipulation ("oromanual") events into characteristic submovements, enabling event-aligned analysis of cortical activity. Activity in forelimb M1 was strongly modulated during food handling, generally higher during oromanual events and lower during holding intervals. Optogenetic silencing and stimulation of forelimb M1 neurons partially affected food-handling movements, exerting suppressive and activating effects, respectively. We also extended the analysis to forelimb S1 and lateral M1, finding broadly similar oromanual-related activity across all three areas. However, each area's activity displayed a distinct timing and phasic/tonic temporal profile, which was further analyzed by non-negative matrix factorization and demonstrated to be attributable to area-specific composition of activity classes. Current or future forelimb position could be accurately predicted from activity in all three regions, indicating that the cortical activity in these areas contains high information content about forelimb movements during food handling. These results thus establish that cortical activity during food handling is manipulation specific, distributed, and broadly similar across multiple sensorimotor areas while also exhibiting area- and submovement-specific relationships with the fast kinematic hallmarks of this natural form of complex free-object-handling manual dexterity.
Identifiants
pubmed: 36243014
pii: S0960-9822(22)01545-7
doi: 10.1016/j.cub.2022.09.045
pmc: PMC9691616
mid: NIHMS1840264
pii:
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
4842-4853.e6Subventions
Organisme : NINDS NIH HHS
ID : R01 NS061963
Pays : United States
Organisme : NINDS NIH HHS
ID : R21 NS116886
Pays : United States
Informations de copyright
Copyright © 2022 Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests The authors declare no competing interests.
Références
Neuron. 2015 Dec 16;88(6):1121-1135
pubmed: 26687221
Elife. 2019 Nov 18;8:
pubmed: 31736463
Nat Protoc. 2019 May;14(5):1339-1376
pubmed: 30980031
J Neurosci. 2013 Jan 23;33(4):1377-90
pubmed: 23345214
Curr Opin Neurobiol. 2018 Apr;49:33-41
pubmed: 29172091
Science. 2021 Apr 16;372(6539):
pubmed: 33859006
PLoS One. 2014 Feb 10;9(2):e88678
pubmed: 24520413
Neuron. 2019 Oct 9;104(1):11-24
pubmed: 31600508
Nat Neurosci. 2014 Mar;17(3):440-8
pubmed: 24487233
Sci Rep. 2017 Nov 17;7(1):15759
pubmed: 29150620
Nat Rev Neurosci. 2021 Dec;22(12):741-757
pubmed: 34711956
Elife. 2016 Oct 10;5:
pubmed: 27719761
Neuron. 2002 May 30;34(5):841-51
pubmed: 12062029
Nat Biomed Eng. 2018 Jul;2(7):508-521
pubmed: 30906646
Nature. 1999 Oct 21;401(6755):788-91
pubmed: 10548103
Neurosci Lett. 1977 Aug;5(5):259-65
pubmed: 19605004
Sci Adv. 2022 Feb 25;8(8):eabk0231
pubmed: 35213216
PLoS Comput Biol. 2021 Sep 22;17(9):e1009439
pubmed: 34550974
Sci Adv. 2019 Oct 30;5(10):eaay0001
pubmed: 31693007
Neuron. 2022 Jul 6;110(13):2080-2093.e10
pubmed: 35609615
Neuron. 2019 Sep 25;103(6):1034-1043.e5
pubmed: 31402199
Neuron. 2017 Aug 2;95(3):683-696.e11
pubmed: 28735748
Neuron. 2021 Jul 21;109(14):2326-2338.e8
pubmed: 34146469
J Neurosci. 2021 Aug 18;41(33):7029-7047
pubmed: 34244359
Behav Brain Res. 1996 May;77(1-2):135-48
pubmed: 8762164
Neuron. 2017 Feb 8;93(3):480-490
pubmed: 28182904
Lab Anim Sci. 1999 Jun;49(3):319-23
pubmed: 10403450
Nature. 2016 Apr 28;532(7600):459-64
pubmed: 27074502
Elife. 2019 Oct 09;8:
pubmed: 31596230
J Neurosci. 2015 Feb 4;35(5):2293-307
pubmed: 25653383
Cereb Cortex. 2012 Aug;22(8):1904-14
pubmed: 21965441
Neuron. 2016 Oct 19;92(2):372-382
pubmed: 27720486
Nat Commun. 2021 Aug 31;12(1):5188
pubmed: 34465784
Nature. 2022 Mar;603(7901):464-469
pubmed: 35264793
Behav Brain Res. 2020 Mar 2;381:112241
pubmed: 31655097
Sci Adv. 2020 Oct 9;6(41):
pubmed: 33036974
PLoS One. 2020 Jan 15;15(1):e0226774
pubmed: 31940368
Elife. 2015 Dec 02;4:e10774
pubmed: 26633811
Neuron. 2019 Nov 20;104(4):765-780.e3
pubmed: 31587918
Nat Neurosci. 2021 Dec;24(12):1721-1732
pubmed: 34737448
J Neurosci. 2021 Feb 3;41(5):911-919
pubmed: 33443081
Nature. 2020 Jan;577(7790):386-391
pubmed: 31875851
Elife. 2021 Jul 29;10:
pubmed: 34324417
Nat Neurosci. 2018 Sep;21(9):1281-1289
pubmed: 30127430
Elife. 2021 Apr 14;10:
pubmed: 33851917
Nature. 2021 Feb;590(7846):445-450
pubmed: 33408409
Nat Neurosci. 2020 Dec;23(12):1537-1549
pubmed: 33169033
Curr Biol. 2022 May 23;32(10):R482-R493
pubmed: 35609550
Neuroscience. 2020 Dec 1;450:151-160
pubmed: 32771500
J Neurosci. 2015 Sep 30;35(39):13311-22
pubmed: 26424880
Nature. 2021 Jun;594(7861):82-87
pubmed: 34012117
Trends Cogn Sci. 2016 Feb;20(2):121-132
pubmed: 26628112
Nature. 2021 Oct;598(7879):86-102
pubmed: 34616075
J Neurosci. 2019 Jan 16;39(3):485-502
pubmed: 30478035
Sci Adv. 2019 Jul 10;5(7):eaaw5388
pubmed: 31309153
J Neurophysiol. 2021 Dec 1;126(6):2065-2090
pubmed: 34788137
Nat Neurosci. 2021 Sep;24(9):1256-1269
pubmed: 34267392
Cell Rep. 2021 Sep 28;36(13):109730
pubmed: 34592148
Nat Neurosci. 2012 Mar 25;15(5):793-802
pubmed: 22446880
PLoS Biol. 2005 May;3(5):e159
pubmed: 15836427
Brain Res. 1984 Feb 6;292(2):251-60
pubmed: 6692158
J Vis Exp. 2010 Jul 21;(41):
pubmed: 20689506