AutoRG: An automatized reach-to-grasp platform technology for assessing forelimb motor function, neural circuit activation, and cognition in rodents.
Immediate early gene
Motor circuitry
Open-source
Reach-to-grasp
Rodents
Volumetric brain imaging
Journal
Journal of neuroscience methods
ISSN: 1872-678X
Titre abrégé: J Neurosci Methods
Pays: Netherlands
ID NLM: 7905558
Informations de publication
Date de publication:
01 03 2023
01 03 2023
Historique:
received:
21
11
2022
revised:
13
01
2023
accepted:
18
01
2023
pubmed:
23
1
2023
medline:
3
3
2023
entrez:
22
1
2023
Statut:
ppublish
Résumé
Rodent reach-to-grasp function assessment is a translationally powerful model for evaluating neurological function impairments and recovery responses. Existing assessment platforms are experimenter-dependent, costly, or low-throughput with limited output measures. Further, a direct histologic comparison of neural activation has never been conducted between any novel, automated platform and the well-established single pellet skilled reach task (SRT). To address these technological and knowledge gaps, we designed an open-source, low-cost Automatized Reach-to-Grasp (AutoRG) pull platform that reduces experimenter interventions and variability. We assessed reach-to-grasp function in rats across seven progressively difficult stages using AutoRG. We mapped AutoRG and SRT-activated motor circuitries in the rat brain using volumetric imaging of the immediate early gene-encoded Arc (activity-regulated cytoskeleton-associated) protein. Rats demonstrated robust forelimb reaching and pulling behavior after training in AutoRG. Reliable force versus time responses were recorded for individual reach events in real time, which were used to derive several secondary functional measures of performance. Moreover, we provide the first demonstration that for a training period of 30 min, AutoRG and SRT both engage similar neural responses in the caudal forelimb area (CFA), rostral forelimb area (RFA), and sensorimotor area (S1). AutoRG is the first low-cost, open-source pull system designed for the scale-up of volitional forelimb motor function testing and characterization of rodent reaching behavior. The similarities in neuronal activation patterns observed in the rat motor cortex after SRT and AutoRG assessments validate the AutoRG as a rigorously characterized, scalable alternative to the conventional SRT and expensive commercial systems.
Sections du résumé
BACKGROUND
Rodent reach-to-grasp function assessment is a translationally powerful model for evaluating neurological function impairments and recovery responses. Existing assessment platforms are experimenter-dependent, costly, or low-throughput with limited output measures. Further, a direct histologic comparison of neural activation has never been conducted between any novel, automated platform and the well-established single pellet skilled reach task (SRT).
NEW METHOD
To address these technological and knowledge gaps, we designed an open-source, low-cost Automatized Reach-to-Grasp (AutoRG) pull platform that reduces experimenter interventions and variability. We assessed reach-to-grasp function in rats across seven progressively difficult stages using AutoRG. We mapped AutoRG and SRT-activated motor circuitries in the rat brain using volumetric imaging of the immediate early gene-encoded Arc (activity-regulated cytoskeleton-associated) protein.
RESULTS
Rats demonstrated robust forelimb reaching and pulling behavior after training in AutoRG. Reliable force versus time responses were recorded for individual reach events in real time, which were used to derive several secondary functional measures of performance. Moreover, we provide the first demonstration that for a training period of 30 min, AutoRG and SRT both engage similar neural responses in the caudal forelimb area (CFA), rostral forelimb area (RFA), and sensorimotor area (S1).
CONCLUSION
AutoRG is the first low-cost, open-source pull system designed for the scale-up of volitional forelimb motor function testing and characterization of rodent reaching behavior. The similarities in neuronal activation patterns observed in the rat motor cortex after SRT and AutoRG assessments validate the AutoRG as a rigorously characterized, scalable alternative to the conventional SRT and expensive commercial systems.
Identifiants
pubmed: 36682731
pii: S0165-0270(23)00017-1
doi: 10.1016/j.jneumeth.2023.109798
pmc: PMC10071513
mid: NIHMS1870926
pii:
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
109798Subventions
Organisme : NINDS NIH HHS
ID : R01 NS099596
Pays : United States
Informations de copyright
Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of Competing Interest None.
Références
J Neurosci Methods. 2015 May 15;246:30-7
pubmed: 25769277
Behav Brain Res. 2015 Mar 15;281:137-48
pubmed: 25523027
Behav Brain Res. 2020 Mar 2;381:112352
pubmed: 31722240
Ann N Y Acad Sci. 2013 Dec;1305:63-71
pubmed: 23841584
Nat Neurosci. 2014 Jul;17(7):995-1002
pubmed: 24908102
eNeuro. 2021 Oct 27;8(5):
pubmed: 34625461
PLoS One. 2015 Oct 27;10(10):e0141254
pubmed: 26506434
J Vis Exp. 2019 Jul 10;(149):
pubmed: 31355787
Cell. 2014 Nov 6;159(4):896-910
pubmed: 25417164
J Vis Exp. 2008 Aug 08;(18):
pubmed: 19066506
Neurobiol Aging. 2016 Jul;43:111-8
pubmed: 27255820
Neuroreport. 2014 Jun 18;25(9):676-82
pubmed: 24818637
Cell. 2016 Jun 16;165(7):1789-1802
pubmed: 27238021
Science. 2015 Aug 28;349(6251):aac4716
pubmed: 26315443
Behav Brain Res. 1989 Feb 1;32(1):11-21
pubmed: 2930630
Behav Brain Res. 1984 Oct;14(1):61-8
pubmed: 6097287
Behav Brain Res. 1991 Jan 31;42(1):77-91
pubmed: 2029348
eNeuro. 2019 Oct 22;6(5):
pubmed: 31540998
Front Behav Neurosci. 2018 Jan 04;11:255
pubmed: 29354039
Cell. 2014 Sep 25;159(1):21-32
pubmed: 25259917
Behav Brain Res. 2016 Feb 15;299:59-71
pubmed: 26611563
Behav Brain Res. 1996 May;77(1-2):135-48
pubmed: 8762164
Front Integr Neurosci. 2018 Aug 03;12:30
pubmed: 30123115
J Neurosci. 2014 Nov 26;34(48):15836-50
pubmed: 25429126
Neurorehabil Neural Repair. 2017 Feb;31(2):122-132
pubmed: 27530125
J Neurophysiol. 2004 Apr;91(4):1832-9
pubmed: 14602838
Exp Brain Res. 2003 Apr;149(4):458-69
pubmed: 12677326
Behav Brain Res. 2009 Dec 1;204(1):153-61
pubmed: 19520119
Exp Neurol. 2021 Jun;340:113672
pubmed: 33652030
Front Neurol. 2014 Jun 20;5:103
pubmed: 24999340
J Neurosci Methods. 2013 Jan 30;212(2):329-37
pubmed: 23183016
Sci Transl Med. 2016 Jun 1;8(341):341ps12
pubmed: 27252173
Neuroscience. 2013 Oct 10;250:557-64
pubmed: 23876329
Neurorehabil Neural Repair. 2019 Jul;33(7):503-512
pubmed: 31189409
Behav Brain Res. 1990 Dec 7;41(1):49-59
pubmed: 2073355
Behav Brain Res. 1992 Mar 15;47(1):59-70
pubmed: 1571101
Brain Res. 1988 Jun 7;451(1-2):97-114
pubmed: 3251605
Neuroscience. 1993 Sep;56(1):33-43
pubmed: 8232915
Annu Rev Neurosci. 2003;26:133-79
pubmed: 14527268
J Neurosci. 1999 Mar 1;19(5):1885-94
pubmed: 10024372
Nature. 2009 Dec 17;462(7275):915-9
pubmed: 19946267
J Neurosci Methods. 1991 Feb;36(2-3):219-28
pubmed: 2062117
Nature. 2014 Jan 30;505(7485):612-3
pubmed: 24482835
Nat Protoc. 2020 Mar;15(3):1237-1254
pubmed: 32034393
J Vis Exp. 2017 Sep 28;(127):
pubmed: 28994796
Neuropsychologia. 1989;27(1):61-9
pubmed: 2710317
Behav Brain Res. 1992 Nov 30;52(1):45-8
pubmed: 1472286
Exp Neurol. 2009 Jul;218(1):145-53
pubmed: 19409894
Curr Biol. 2019 Nov 4;29(21):3551-3562.e7
pubmed: 31630947
Front Neurol. 2014 Jul 07;5:116
pubmed: 25071704
J Neurosci Methods. 2016 Sep 15;271:119-27
pubmed: 27450925
Neuron. 2015 Jun 17;86(6):1385-92
pubmed: 26051420
Neuroscience. 1999 Jan;88(2):629-42
pubmed: 10197781
eNeuro. 2020 Oct 21;7(5):
pubmed: 33008812
J Neural Eng. 2021 Aug 31;18(4):
pubmed: 34407518
J Neurosci. 2014 May 7;34(19):6583-95
pubmed: 24806683
Physiol Behav. 1992 Jun;51(6):1151-6
pubmed: 1641415
J Neurosci Methods. 2016 Jun 15;266:11-20
pubmed: 26976724
Neurobiol Dis. 2013 Dec;60:80-8
pubmed: 23954448
J Neurosci Methods. 2016 Jan 30;258:16-23
pubmed: 26484787
Behav Brain Res. 2018 Apr 16;342:1-10
pubmed: 29307665
Behav Neurosci. 1996 Feb;110(1):117-25
pubmed: 8652060
Nat Commun. 2019 Dec 19;10(1):5782
pubmed: 31857587
IEEE Trans Neural Syst Rehabil Eng. 2013 Sep;21(5):796-805
pubmed: 23335672
J Neurosci Methods. 2013 Mar 30;214(1):52-61
pubmed: 23353133
Brain Res. 1982 Jan 28;232(1):151-6
pubmed: 7055691