Mathematical relationships between spinal motoneuron properties.

Henneman's size principle mathematical relationships motoneuron motor neuron motor neuron size motor unit neuroscience none physics of living systems

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
18 07 2022
Historique:
received: 17 12 2021
accepted: 13 07 2022
pubmed: 19 7 2022
medline: 1 11 2022
entrez: 18 7 2022
Statut: epublish

Résumé

Our understanding of the behaviour of spinal alpha-motoneurons (MNs) in mammals partly relies on our knowledge of the relationships between MN membrane properties, such as MN size, resistance, rheobase, capacitance, time constant, axonal conduction velocity, and afterhyperpolarization duration. We reprocessed the data from 40 experimental studies in adult cat, rat, and mouse MN preparations to empirically derive a set of quantitative mathematical relationships between these MN electrophysiological and anatomical properties. This validated mathematical framework, which supports past findings that the MN membrane properties are all related to each other and clarifies the nature of their associations, is besides consistent with the Henneman's size principle and Rall's cable theory. The derived mathematical relationships provide a convenient tool for neuroscientists and experimenters to complete experimental datasets, explore the relationships between pairs of MN properties never concurrently observed in previous experiments, or investigate inter-mammalian-species variations in MN membrane properties. Using this mathematical framework, modellers can build profiles of inter-consistent MN-specific properties to scale pools of MN models, with consequences on the accuracy and the interpretability of the simulations. Muscles receive their instructions through electrical signals carried by tens or hundreds of cells connected to the command centers of the body. These ‘alpha-motoneurons’ have various sizes and electrical characteristics which affect how they transmit signals. Previous experiments have shown that these properties are linked; for instance, larger motoneurons transfer electrical signals more quickly. The exact nature of the mathematical relationships between these characteristics, however, remains unclear. This limits our understanding of the behaviour of motoneurons from experimental data. To identify the equations linking eight motoneuron properties, Caillet et al. analysed published datasets from experimental studies on cat motoneurons. This approach uncovered simple mathematical associations: in fact, only one characteristic needs to be measured experimentally to calculate all the other properties. The relationships identified were also consistent with previously accepted approaches for modelling motoneuron activity. Caillet et al. then validated this mathematical framework with data from studies on rodents, showing that some of the equations hold true for different mammals. This work offers a quick and easy way for researchers to calculate the characteristics of a motoneuron based on a single observation. This will allow non-measured properties to be added to experimental datasets, and it could help to uncover the diversity of motoneurons at work within a population.

Autres résumés

Type: plain-language-summary (eng)
Muscles receive their instructions through electrical signals carried by tens or hundreds of cells connected to the command centers of the body. These ‘alpha-motoneurons’ have various sizes and electrical characteristics which affect how they transmit signals. Previous experiments have shown that these properties are linked; for instance, larger motoneurons transfer electrical signals more quickly. The exact nature of the mathematical relationships between these characteristics, however, remains unclear. This limits our understanding of the behaviour of motoneurons from experimental data. To identify the equations linking eight motoneuron properties, Caillet et al. analysed published datasets from experimental studies on cat motoneurons. This approach uncovered simple mathematical associations: in fact, only one characteristic needs to be measured experimentally to calculate all the other properties. The relationships identified were also consistent with previously accepted approaches for modelling motoneuron activity. Caillet et al. then validated this mathematical framework with data from studies on rodents, showing that some of the equations hold true for different mammals. This work offers a quick and easy way for researchers to calculate the characteristics of a motoneuron based on a single observation. This will allow non-measured properties to be added to experimental datasets, and it could help to uncover the diversity of motoneurons at work within a population.

Identifiants

pubmed: 35848819
doi: 10.7554/eLife.76489
pii: 76489
pmc: PMC9612914
doi:
pii:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2022, Caillet et al.

Déclaration de conflit d'intérêts

AC, AP, DF, LM No competing interests declared

Références

J Physiol. 1958 Aug 29;143(1):11-40
pubmed: 13576457
Pediatr Diabetes. 2006 Oct;7(5):284-8
pubmed: 17054451
J Physiol. 2001 Apr 1;532(Pt 1):271-81
pubmed: 11283241
Nature. 1957 Apr 27;179(4565):866-8
pubmed: 13430719
J Neurophysiol. 1990 Oct;64(4):1339-46
pubmed: 2258751
PLoS Comput Biol. 2022 Sep 29;18(9):e1010556
pubmed: 36174126
J Physiol. 1979 Feb;287:33-43
pubmed: 430414
J Neurophysiol. 1987 Jun;57(6):1730-45
pubmed: 3598628
J Neurophysiol. 1993 Apr;69(4):1160-70
pubmed: 8492155
J Physiol. 1989 May;412:1-21
pubmed: 2600827
Neurosci Lett. 2000 Aug 11;289(3):217-20
pubmed: 10961668
J Physiol. 1955 Nov 28;130(2):291-325
pubmed: 13278904
J Physiol. 1973 Apr;230(2):359-70
pubmed: 4350770
Brain Res. 1981 Jan 12;204(2):311-26
pubmed: 7459634
Brain Res. 1974 Feb 15;67(1):89-101
pubmed: 4470419
Int J Dev Neurosci. 2003 Dec;21(8):461-9
pubmed: 14659997
J Neurophysiol. 1998 Aug;80(2):583-93
pubmed: 9705452
J Neurophysiol. 2012 Jan;107(2):728-41
pubmed: 22031766
J Neurophysiol. 1992 Mar;67(3):508-29
pubmed: 1578242
J Neurophysiol. 1965 Jan;28:71-84
pubmed: 14244797
J Neurophysiol. 2002 Jul;88(1):265-76
pubmed: 12091552
J Physiol. 2008 Jan 15;586(2):529-44
pubmed: 18006586
J Physiol. 1992 Mar;448:677-95
pubmed: 1593483
Elife. 2018 Mar 27;7:
pubmed: 29580378
Exp Neurol. 1986 Jul;93(1):227-52
pubmed: 3732460
J Neurophysiol. 2010 Sep;104(3):1549-65
pubmed: 20592119
Neurosci Lett. 1978 Apr;8(1):17-20
pubmed: 19605142
Exp Neurol. 1959 Nov;1:491-527
pubmed: 14435979
J Neurophysiol. 1985 May;53(5):1323-44
pubmed: 3839011
Neurosci Lett. 1980 Oct 2;19(3):303-7
pubmed: 7052536
Neuroscience. 2006 May 12;139(2):531-8
pubmed: 16460880
J Neurol Neurosurg Psychiatry. 1971 Apr;34(2):113-20
pubmed: 4255199
J Physiol. 1974 Jun;239(2):301-24
pubmed: 4137933
Exp Neurol. 1960 Oct;2:503-32
pubmed: 13739270
J Neurophysiol. 1999 Apr;81(4):1718-29
pubmed: 10200207
Proc R Soc Lond B Biol Sci. 1975 Apr 29;189(1094):81-6
pubmed: 237279
Exp Neurol. 1971 Mar;30(3):475-83
pubmed: 4251992
J Physiol. 1968 Jun;196(3):631-54
pubmed: 5664235
J Neurophysiol. 1965 May;28:560-80
pubmed: 14328454
J Neurophysiol. 2010 May;103(5):2833-45
pubmed: 20457856
J Neurophysiol. 1966 Mar;29(2):207-20
pubmed: 5927458
J Physiol. 1965 Oct;180(3):607-35
pubmed: 5846796
J Neurophysiol. 2020 May 1;123(5):1682-1690
pubmed: 32233911
Neurobiol Dis. 2007 Nov;28(2):154-64
pubmed: 17766128
J Physiol. 2014 Apr 1;592(7):1687-703
pubmed: 24445319
Physiol Rev. 1992 Oct;72(4 Suppl):S159-86
pubmed: 1438585
J Physiol. 1984 Nov;356:401-31
pubmed: 6520792
J Comp Neurol. 1982 Jul 20;209(1):17-28
pubmed: 7119171
J Comp Neurol. 1992 Mar 1;317(1):79-90
pubmed: 1573058
J Neurophysiol. 1965 Jan;28:85-99
pubmed: 14244798
J Neurophysiol. 1991 Jun;65(6):1509-16
pubmed: 1875259
J Physiol. 2013 Feb 15;591(4):875-97
pubmed: 23129791
Biophys J. 1998 Feb;74(2 Pt 1):1061-73
pubmed: 9533718
Exp Neurol. 1987 Jan;95(1):142-54
pubmed: 2947808
J Physiol. 1997 Mar 15;499 ( Pt 3):809-23
pubmed: 9130174
J Clin Neurophysiol. 1995 Nov;12(6):538-59
pubmed: 8600170
Nat Commun. 2018 Feb 19;9(1):709
pubmed: 29459723
J Neurophysiol. 2015 Apr 1;113(7):2769-77
pubmed: 25695651
J Comp Neurol. 2010 Oct 15;518(20):4213-25
pubmed: 20878784
J Comp Neurol. 1991 Sep 22;311(4):531-45
pubmed: 1757602
J Physiol. 1984 Dec;357:453-83
pubmed: 6512700
eNeuro. 2021 Mar 22;8(2):
pubmed: 33632815
Anat Histol Embryol. 2014 Jun;43(3):182-9
pubmed: 23617786
J Neurophysiol. 1986 May;55(5):947-65
pubmed: 3711974
Brain Res. 1986 Oct 15;385(1):22-9
pubmed: 3768720
J Physiol. 1974 Apr;238(2):269-78
pubmed: 4840992
J Neurophysiol. 1998 Jan;79(1):371-8
pubmed: 9425206
J Neurophysiol. 2018 Aug 1;120(2):601-609
pubmed: 29718808
J Neurophysiol. 2004 Jun;91(6):2515-23
pubmed: 14724266
J Comp Neurol. 2005 Mar 14;483(3):304-17
pubmed: 15682391
Proc Natl Acad Sci U S A. 2009 Aug 11;106(32):13588-93
pubmed: 19651609
Brain Res. 1975 Jun 27;91(2):177-95
pubmed: 1164670
J Neurophysiol. 1980 Jun;43(6):1615-30
pubmed: 6447772
Exp Brain Res. 1975 Sep 29;23(3):301-13
pubmed: 1183507
Muscle Nerve. 2005 Aug;32(2):119-39
pubmed: 15880485
J Physiol. 1979 Aug;293:197-215
pubmed: 501587
J Electromyogr Kinesiol. 2018 Dec;43:104-110
pubmed: 30267966
Acta Physiol Scand. 1970 Aug;79(4):435-52
pubmed: 5472111
Brain Res. 2009 Sep 29;1291:40-52
pubmed: 19619517
J Physiol. 1952 Aug;117(4):431-60
pubmed: 12991232
J Physiol. 2016 Oct 1;594(19):5491-505
pubmed: 27151459
J Neurophysiol. 1988 Jul;60(1):60-85
pubmed: 3404225
J Neurosci. 1994 Aug;14(8):4613-38
pubmed: 8046439
J Appl Physiol (1985). 1990 Jan;68(1):26-34
pubmed: 2312467
J Physiol. 1958 Jul 14;142(2):275-91
pubmed: 13564435
Brain Res. 1984 Jul 30;307(1-2):167-79
pubmed: 6466992
J Neurophysiol. 2008 Jul;100(1):474-81
pubmed: 18463177
J Neurophysiol. 1989 Aug;62(2):311-24
pubmed: 2769333
J Exp Biol. 1985 Mar;115:105-12
pubmed: 3161974
J Neurophysiol. 1981 Nov;46(5):1076-88
pubmed: 7299447
J Comp Neurol. 2009 May 10;514(2):189-202
pubmed: 19274669
J Neurophysiol. 1981 Dec;46(6):1326-38
pubmed: 6275043
J Neurophysiol. 1992 May;67(5):1385-403
pubmed: 1597721
J Neurosci. 2011 Oct 19;31(42):15188-94
pubmed: 22016552
J Physiol. 1971 Jan;212(1):120
pubmed: 5545177
J Neurophysiol. 1986 Apr;55(4):619-34
pubmed: 3701396
Neural Comput. 2011 Nov;23(11):2833-67
pubmed: 21851282
J Neurol Sci. 1982 Jun;54(3):401-12
pubmed: 7097310
Biophys J. 1969 Dec;9(12):1483-508
pubmed: 5352228
PLoS One. 2014 Mar 25;9(3):e92390
pubmed: 24667744
J Comp Neurol. 1988 Dec 1;278(1):103-20
pubmed: 3209749
J Neurophysiol. 2020 Apr 1;123(4):1380-1391
pubmed: 32073942
Brain Res. 1981 Jan 12;204(2):295-309
pubmed: 7459633
J Neurophysiol. 1974 Nov;37(6):1338-49
pubmed: 4436704
J Physiol. 1991;440:345-66
pubmed: 1804967
J Physiol. 1988 Jun;400:135-58
pubmed: 3418525
Brain Res. 2011 Aug 29;1409:42-61
pubmed: 21762884
J Physiol. 1989 Feb;409:63-87
pubmed: 2585300
IEEE Trans Neural Netw. 2004 Sep;15(5):1063-70
pubmed: 15484883
J Appl Physiol (1985). 2000 Aug;89(2):563-72
pubmed: 10926639
Acta Physiol Scand. 1968 Aug;73(4):471-80
pubmed: 5708174
Brain Struct Funct. 2016 Sep;221(7):3755-86
pubmed: 26476929
J Comp Neurol. 2008 Nov 20;511(3):329-41
pubmed: 18803237
J Neurophysiol. 1996 Jun;75(6):2509-19
pubmed: 8793760
J Comp Neurol. 1981 Nov 10;202(4):571-83
pubmed: 7298916
J Physiol. 1973 Nov;234(3):749-65
pubmed: 4148753
J Neurophysiol. 1987 Apr;57(4):1227-45
pubmed: 3585462
Neuromuscul Disord. 1992;2(4):261-7
pubmed: 1483052
Neuroscience. 2012 May 3;209:144-54
pubmed: 22387111
Brain Res. 1977 Apr 8;125(1):91-7
pubmed: 851876
J Physiol. 1956 Nov 28;134(2):451-70
pubmed: 13398925
J Physiol. 1987 Oct;391:561-71
pubmed: 3443957
J Comp Neurol. 2018 Dec 15;526(18):2973-2983
pubmed: 30411341
J Neurophysiol. 1998 May;79(5):2485-502
pubmed: 9582222
Science. 1966 Jun 17;152(3729):1637-40
pubmed: 5936887
Science. 1957 Dec 27;126(3287):1345-7
pubmed: 13495469
Compr Physiol. 2012 Oct;2(4):2629-82
pubmed: 23720261
J Comp Neurol. 1987 Jan 1;255(1):68-81
pubmed: 3819010
Eur J Neurosci. 1999 Jun;11(6):2093-102
pubmed: 10336678
J Physiol. 2018 May 1;596(9):1723-1745
pubmed: 29502344
Can J Appl Physiol. 1997 Dec;22(6):585-97
pubmed: 9415831
J Physiol. 1993 Apr;463:307-24
pubmed: 8246185
J Neurosci. 2009 Sep 9;29(36):11246-56
pubmed: 19741131
J Membr Biol. 1993 Feb;132(1):27-40
pubmed: 8459447
J Neurophysiol. 1977 Jul;40(4):879-90
pubmed: 886372
Physiology (Bethesda). 2019 Jan 1;34(1):5-13
pubmed: 30540233
J Neurophysiol. 1965 May;28(3):599-620
pubmed: 5835487
Biophys J. 2000 Jul;79(1):314-20
pubmed: 10866957
Rev Physiol Biochem Pharmacol. 2001;143:137-263
pubmed: 11428264
Brain Res. 1975 Oct 10;96(1):114-8
pubmed: 1174992
J Physiol. 1977 Feb;265(1):163-74
pubmed: 850157
Brain Res. 1981 Dec 14;229(1):193-6
pubmed: 7306807
Science. 1957 Sep 6;126(3271):454
pubmed: 13467230

Auteurs

Arnault H Caillet (AH)

Department of Civil and Environmental Engineering, Imperial College London, London, United Kingdom.

Andrew T M Phillips (ATM)

Department of Civil and Environmental Engineering, Imperial College London, London, United Kingdom.

Dario Farina (D)

Department of Bioengineering, Imperial College London, London, United Kingdom.

Luca Modenese (L)

Department of Civil and Environmental Engineering, Imperial College London, London, United Kingdom.
Graduate School of Biomedical Engineering, University of New South Wales, Sydney, Australia.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH