Endurance-exercise training adaptations in spinal motoneurones: potential functional relevance to locomotor output and assessment in humans.
High-density surface EMG
Locomotion
Task-dependent
Journal
European journal of applied physiology
ISSN: 1439-6327
Titre abrégé: Eur J Appl Physiol
Pays: Germany
ID NLM: 100954790
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
07
07
2021
accepted:
11
02
2022
pubmed:
1
3
2022
medline:
28
5
2022
entrez:
28
2
2022
Statut:
ppublish
Résumé
It is clear from non-human animal work that spinal motoneurones undergo endurance training (chronic) and locomotor (acute) related changes in their electrical properties and thus their ability to fire action potentials in response to synaptic input. The functional implications of these changes, however, are speculative. In humans, data suggests that similar chronic and acute changes in motoneurone excitability may occur, though the work is limited due to technical constraints. To examine the potential influence of chronic changes in human motoneurone excitability on the acute changes that occur during locomotor output, we must develop more sophisticated recording techniques or adapt our current methods. In this review, we briefly discuss chronic and acute changes in motoneurone excitability arising from non-human and human work. We then discuss the potential interaction effects of chronic and acute changes in motoneurone excitability and the potential impact on locomotor output. Finally, we discuss the use of high-density surface electromyogram recordings to examine human motor unit firing patterns and thus, indirectly, motoneurone excitability. The assessment of single motor units from high-density recording is mainly limited to tonic motor outputs and minimally dynamic motor output such as postural sway. Adapting this technology for use during locomotor outputs would allow us to gain a better understanding of the potential functional implications of endurance training-induced changes in human motoneurone excitability on motor output.
Identifiants
pubmed: 35226169
doi: 10.1007/s00421-022-04918-2
pii: 10.1007/s00421-022-04918-2
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1367-1381Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Adam A, Luca CJD, Erim Z (1998) Hand dominance and motor unit firing behavior. J Neurophysiol 80:1373–1382. https://doi.org/10.1152/jn.1998.80.3.1373
doi: 10.1152/jn.1998.80.3.1373
pubmed: 9744946
Beaumont E, Gardiner P (2002) Effects of daily spontaneous running on the electrophysiological properties of hindlimb motoneurones in rats. J Physiol 540:129–138. https://doi.org/10.1113/jphysiol.2001.013084
doi: 10.1113/jphysiol.2001.013084
pubmed: 11927675
pmcid: 2290217
Beaumont E, Gardiner PF (2003) Endurance training alters the biophysical properties of hindlimb motoneurons in rats. Muscle Nerve 27:228–236. https://doi.org/10.1002/mus.10308
doi: 10.1002/mus.10308
pubmed: 12548531
Beaumont E, Houlé JD, Peterson CA, Gardiner PF (2004) Passive exercise and fetal spinal cord transplant both help to restore motoneuronal properties after spinal cord transection in rats. Muscle Nerve 29:234–242. https://doi.org/10.1002/mus.10539
doi: 10.1002/mus.10539
pubmed: 14755488
Borzelli D, Gazzoni M, Botter A et al (2020) Contraction level, but not force direction or wrist position, affects the spatial distribution of motor unit recruitment in the biceps brachii muscle. Eur J Appl Physiol 120:853–860. https://doi.org/10.1007/s00421-020-04324-6
doi: 10.1007/s00421-020-04324-6
pubmed: 32076830
Brownstone RM, Jordan LM, Kriellaars DJ et al (1992) On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat. Exp Brain Res. https://doi.org/10.1007/BF00230927
doi: 10.1007/BF00230927
pubmed: 1426105
Brownstone RM (2006) Beginning at the end: Repetitive firing properties in the final common pathway. Prog Neurobiol 78:156–172. https://doi.org/10.1016/j.pneurobio.2006.04.002
Brownstone RM, Krawitz S, Jordan LM (2011) Reversal of the late phase of spike frequency adaptation in cat spinal motoneurons during fictive locomotion. J Neurophysiol 105:1045–1050. https://doi.org/10.1152/jn.00411.2010
Button DC, Gardiner K, Marqueste T, Gardiner PF (2006) Frequency–current relationships of rat hindlimb α-motoneurones. J Physiol 573:663–677. https://doi.org/10.1113/jphysiol.2006.107292
doi: 10.1113/jphysiol.2006.107292
pubmed: 16613880
pmcid: 1779753
Button DC, Kalmar JM, Gardiner K et al (2007) Spike frequency adaptation of rat hindlimb motoneurons. J Appl Physiol 102:1041–1050. https://doi.org/10.1152/japplphysiol.01148.2006
doi: 10.1152/japplphysiol.01148.2006
pubmed: 17158244
Chen M, Zhou P (2016) A novel framework based on FastICA for high density surface EMG decomposition. IEEE Trans Neural Syst Rehabil Eng 24:117–127. https://doi.org/10.1109/TNSRE.2015.2412038
doi: 10.1109/TNSRE.2015.2412038
pubmed: 25775496
Cogliati M, Cudicio A, Martinez-Valdes E et al (2020) Half marathon induces changes in central control and peripheral properties of individual motor units in master athletes. J Electromyogr Kinesiol 55:102472. https://doi.org/10.1016/j.jelekin.2020.102472
doi: 10.1016/j.jelekin.2020.102472
pubmed: 32987340
Copithorne DB, Forman DA, Power KE (2015) Premovement Changes in Corticospinal Excitability of the Biceps Brachii are Not Different Between Arm Cycling and an Intensity-Matched Tonic Contraction. Motor Control 19:223–241. https://doi.org/10.1123/mc.2014-0022
Cohen JW, Vieira T, Ivanova TD et al (2021) Maintenance of standing posture during multi-directional leaning demands the recruitment of task-specific motor units in the ankle plantarflexors. Exp Brain Res 239:2569–2581. https://doi.org/10.1007/s00221-021-06154-0
doi: 10.1007/s00221-021-06154-0
pubmed: 34191118
Collins BW, Button DC (2018) The effect of shoulder position on motor evoked and maximal muscle compound action potentials of the biceps brachii. Neurosci Lett 665:206–211. https://doi.org/10.1016/j.neulet.2017.12.019
doi: 10.1016/j.neulet.2017.12.019
pubmed: 29229395
Dai Y, Jones KE, Fedirchuk B et al (2002) A modelling study of locomotion-induced hyperpolarization of voltage threshold in cat lumbar motoneurones. J Physiol 544:521–536. https://doi.org/10.1113/jphysiol.2002.026005
doi: 10.1113/jphysiol.2002.026005
pubmed: 12381824
pmcid: 2290604
De Luca CJ, Chang SS, Roy SH et al (2015) Decomposition of surface EMG signals from cyclic dynamic contractions. J Neurophysiol 113:1941–1951. https://doi.org/10.1152/jn.00555.2014
doi: 10.1152/jn.00555.2014
pubmed: 25540220
Desmedt JE, Godaux E (1979) Voluntary motor commands in human ballistic movements. Ann Neurol 5:415–421. https://doi.org/10.1002/ana.410050503
doi: 10.1002/ana.410050503
pubmed: 464547
Farina D, Holobar A (2016) Characterization of human motor units from surface EMG decomposition. Proc IEEE 104:353–373. https://doi.org/10.1109/JPROC.2015.2498665
doi: 10.1109/JPROC.2015.2498665
Farina D, Merletti R (2001) A novel approach for precise simulation of the EMG signal detected by surface electrodes. IEEE Trans Biomed Eng 48:637–646. https://doi.org/10.1109/10.923782
doi: 10.1109/10.923782
pubmed: 11396594
Farina D, Cescon C, Merletti R (2002) Influence of anatomical, physical, and detection-system parameters on surface EMG. Biol Cybern 86:445–456. https://doi.org/10.1007/s00422-002-0309-2
doi: 10.1007/s00422-002-0309-2
pubmed: 12111273
Farina D, Negro F, Gazzoni M, Enoka RM (2008) Detecting the unique representation of motor-unit action potentials in the surface electromyogram. J Neurophysiol 100:1223–1233. https://doi.org/10.1152/jn.90219.2008
doi: 10.1152/jn.90219.2008
pubmed: 18497352
pmcid: 2544462
Farup J, Kjølhede T, Sørensen H et al (2012) Muscle morphological and strength adaptations to endurance vs. resistance training. J Strength Cond Res 26:398–407. https://doi.org/10.1519/JSC.0b013e318225a26f
doi: 10.1519/JSC.0b013e318225a26f
pubmed: 22266546
Forman D, Raj A, Button DC, Power KE (2014) Corticospinal excitability of the biceps brachii is higher during arm cycling than an intensity-matched tonic contraction. J Neurophysiol 112:1142–1151. https://doi.org/10.1152/jn.00210.2014
doi: 10.1152/jn.00210.2014
pubmed: 24899677
Forman DA, Monks M, Power KE (2019) Corticospinal excitability, assessed through stimulus response curves, is phase-, task-, and muscle-dependent during arm cycling. Neuroscience Letters 692:100–106. https://doi.org/10.1016/j.neulet.2018.11.003
Franchi MV, Wilkinson DJ, Quinlan JI et al (2015) Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle. Physiol Rep 3:e12593. https://doi.org/10.14814/phy2.12593
doi: 10.14814/phy2.12593
pubmed: 26564061
pmcid: 4673627
Gallina A, Vieira T (2015) Territory and fiber orientation of vastus medialis motor units: a surface electromyography investigation. Muscle Nerve 52:1057–1065. https://doi.org/10.1002/mus.24662
doi: 10.1002/mus.24662
pubmed: 25808985
Gardiner P, Beaumont E, Cormery B (2005) Motoneurones “learn” and “forget” physical activity. Can J Appl Physiol 30:352–370. https://doi.org/10.1139/h05-127
doi: 10.1139/h05-127
pubmed: 16129890
Gardiner P, Dai Y, Heckman CJ (2006) Effects of exercise training on α-motoneurons. J Appl Physiol 101:1228–1236. https://doi.org/10.1152/japplphysiol.00482.2006
doi: 10.1152/japplphysiol.00482.2006
pubmed: 16778002
Ge R, Dai Y (2020) Three-week treadmill exercise enhances persistent inward currents, facilitates dendritic plasticity, and upregulates the excitability of dorsal raphe serotonin neurons in ePet-EYFP mice. Front Cell Neurosci. https://doi.org/10.3389/fncel.2020.575626
doi: 10.3389/fncel.2020.575626
pubmed: 33613195
pmcid: 7793874
Gilmore J, Fedirchuk B (2004) The excitability of lumbar motoneurones in the neonatal rat is increased by a hyperpolarization of their voltage threshold for activation by descending serotonergic fibres: descending 5-HT fibres hyperpolarize V
doi: 10.1113/jphysiol.2004.064717
pubmed: 15121804
pmcid: 1664930
Glaser V, Holobar A (2019) Motor unit identification from high-density surface electromyograms in repeated dynamic muscle contractions. IEEE Trans Neural Syst Rehabil Eng 27:66–75. https://doi.org/10.1109/TNSRE.2018.2885283
doi: 10.1109/TNSRE.2018.2885283
pubmed: 30571641
Gómez-Pinilla F, Ying Z, Opazo P et al (2001) Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur J Neurosci 13:1078–1084. https://doi.org/10.1046/j.0953-816x.2001.01484.x
doi: 10.1046/j.0953-816x.2001.01484.x
pubmed: 11285004
Gómez-Pinilla F, Ying Z, Roy RR et al (2002) Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 88:2187–2195. https://doi.org/10.1152/jn.00152.2002
doi: 10.1152/jn.00152.2002
pubmed: 12424260
Gorassini M, Yang JF, Siu M, Bennett DJ (2002) Intrinsic activation of human motoneurons: possible contribution to motor unit excitation. J Neurophysiol 87:1850–1858. https://doi.org/10.1152/jn.00024.2001
doi: 10.1152/jn.00024.2001
pubmed: 11929906
Hamilton MT, Booth FW (2000) Skeletal muscle adaptation to exercise: a century of progress. J Appl Physiol 88:327–331. https://doi.org/10.1152/jappl.2000.88.1.327
doi: 10.1152/jappl.2000.88.1.327
pubmed: 10642397
Hamilton LD, Mani D, Almuklass AM et al (2018) Electrical nerve stimulation modulates motor unit activity in contralateral biceps brachii during steady isometric contractions. J Neurophysiol 120:2603–2613. https://doi.org/10.1152/jn.00235.2018
doi: 10.1152/jn.00235.2018
pubmed: 30156959
Heckman CJ, Lee RH, Brownstone RM (2003) Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci 26:688–695. https://doi.org/10.1016/j.tins.2003.10.002
doi: 10.1016/j.tins.2003.10.002
pubmed: 14624854
Holobar A, Zazula D (2007) Multichannel blind source separation using convolution kernel compensation. IEEE Trans Signal Process 55:4487–4496. https://doi.org/10.1109/TSP.2007.896108
doi: 10.1109/TSP.2007.896108
Holobar A, Farina D, Gazzoni M et al (2009) Estimating motor unit discharge patterns from high-density surface electromyogram. Clin Neurophysiol 120:551–562. https://doi.org/10.1016/j.clinph.2008.10.160
doi: 10.1016/j.clinph.2008.10.160
pubmed: 19208498
Holobar A, Minetto MA, Botter A et al (2010) Experimental analysis of accuracy in the identification of motor unit spike trains from high-density surface EMG. IEEE Trans Neural Syst Rehabil Eng. https://doi.org/10.1109/TNSRE.2010.2041593
doi: 10.1109/TNSRE.2010.2041593
pubmed: 20144921
Hughes DC, Ellefsen S, Baar K (2018) Adaptations to endurance and strength training. Cold Spring Harb Perspect Med 8:1–17. https://doi.org/10.1101/cshperspect.a029769
doi: 10.1101/cshperspect.a029769
Illera-Domínguez V, Nuell S, Carmona G et al (2018) Early functional and morphological muscle adaptations during short-term inertial-squat training. Front Physiol 9:1–12. https://doi.org/10.3389/fphys.2018.01265
doi: 10.3389/fphys.2018.01265
Kalmar JM (2018) On task: considerations and future directions for studies of corticospinal excitability in exercise neuroscience and related disciplines. Appl Physiol Nutr Metab 43:1113–1121. https://doi.org/10.1139/apnm-2018-0123
doi: 10.1139/apnm-2018-0123
pubmed: 29701483
Krawitz S, Fedirchuk B, Dai Y et al (2001) State-dependent hyperpolarization of voltage threshold enhances motoneurone excitability during fictive locomotion in the cat. J Physiol 532:271–281. https://doi.org/10.1111/j.1469-7793.2001.0271g.x
doi: 10.1111/j.1469-7793.2001.0271g.x
pubmed: 11283241
pmcid: 2278523
Lockyer EJ, Benson RJ, Hynes AP et al (2018) Intensity matters: effects of cadence and power output on corticospinal excitability during arm cycling are phase and muscle dependent. J Neurophysiol 120:2908–2921. https://doi.org/10.1152/jn.00358.2018
doi: 10.1152/jn.00358.2018
pubmed: 30354778
pmcid: 6337038
Lockyer EJ, Compton CT, Forman DA et al (2021) Moving forward: methodological considerations when assessing corticospinal excitability during rhythmic motor output in humans. J Neurophysiol. https://doi.org/10.1152/jn.00027.2021
doi: 10.1152/jn.00027.2021
pubmed: 34133230
Lowery MM, Stoykov NS, Dewald JPA, Kuiken TA (2004) Volume conduction in an anatomically based surface EMG model. IEEE Trans Biomed Eng 51:2138–2147. https://doi.org/10.1109/TBME.2004.836494
doi: 10.1109/TBME.2004.836494
pubmed: 15605861
MacDonell CW, Gardiner PF (2018) Mechanisms and functional implications of motoneuron adaptations to increased physical activity. Appl Physiol Nutr Metab 43:1186–1193. https://doi.org/10.1139/apnm-2018-0185
doi: 10.1139/apnm-2018-0185
pubmed: 29856929
MacDonell CW, Button DC, Beaumont E et al (2012) Plasticity of rat motoneuron rhythmic firing properties with varying levels of afferent and descending inputs. J Neurophysiol 107:265–272. https://doi.org/10.1152/jn.00122.2011
doi: 10.1152/jn.00122.2011
pubmed: 21957225
MacDonell CW, Power KE, Chopek JW et al (2015) Extensor motoneurone properties are altered immediately before and during fictive locomotion in the adult decerebrate rat: motoneurone properties during fictive locomotion. J Physiol 593:2327–2342. https://doi.org/10.1113/JP270239
doi: 10.1113/JP270239
pubmed: 25809835
pmcid: 4457195
Martinez-Valdes E, Falla D, Negro F et al (2017a) Differential motor unit changes after endurance or high-intensity interval training. Med Sci Sports Exerc 49:1126–1136. https://doi.org/10.1249/MSS.0000000000001209
doi: 10.1249/MSS.0000000000001209
pubmed: 28121801
Martinez-Valdes E, Negro F, Laine CM et al (2017b) Tracking motor units longitudinally across experimental sessions with high-density surface electromyography: motor unit tracking with high-density EMG. J Physiol 595:1479–1496. https://doi.org/10.1113/JP273662
doi: 10.1113/JP273662
pubmed: 28032343
pmcid: 5330923
Martinez-Valdes E, Farina D, Negro F et al (2018) Early motor unit conduction velocity changes to high-intensity interval training versus continuous training. Med Sci Sports Exerc 50:2339–2350. https://doi.org/10.1249/MSS.0000000000001705
doi: 10.1249/MSS.0000000000001705
pubmed: 29975302
McNeil CJ, Butler JE, Taylor JL, Gandevia SC (2013) Testing the excitability of human motoneurons. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2013.00152
doi: 10.3389/fnhum.2013.00152
pubmed: 23630483
pmcid: 3633937
Nawab SH, Chang SS, De Luca CJ (2010) High-yield decomposition of surface EMG signals. Clin Neurophysiol 121:1602–1615. https://doi.org/10.1016/j.clinph.2009.11.092
doi: 10.1016/j.clinph.2009.11.092
pubmed: 20430694
pmcid: 2932793
Negro F, Muceli S, Castronovo AM et al (2016) Multi-channel intramuscular and surface EMG decomposition by convolutive blind source separation. J Neural Eng 13:26027. https://doi.org/10.1088/1741-2560/13/2/026027
doi: 10.1088/1741-2560/13/2/026027
Perreault M-C (2002) Motoneurons Have Different Membrane Resistance during Fictive Scratching and Weight Support. J Neurosci 22:8259–8265. https://doi.org/10.1523/JNEUROSCI.22-18-08259.2002
Potvin JR (1997) Effects of muscle kinematics on surface EMG amplitude and frequency during fatiguing dynamic contractions. J Appl Physiol (1985) 82:144–151. https://doi.org/10.1152/jappl.1997.82.1.144
doi: 10.1152/jappl.1997.82.1.144
Power KE, McCrea DA, Fedirchuk B (2010) Intraspinally mediated state-dependent enhancement of motoneurone excitability during fictive scratch in the adult decerebrate cat: intraspinal regulation of motoneurone excitability during fictive scratch. J Physiol 588:2839–2857. https://doi.org/10.1113/jphysiol.2010.188722
doi: 10.1113/jphysiol.2010.188722
pubmed: 20547677
pmcid: 2956902
Power KE, Copithorne DB (2013) Increased corticospinal excitability prior to arm cycling is due to enhanced supraspinal but not spinal motoneurone excitability. Appl Physiol Nutr Metab 38:1154–1161. https://doi.org/10.1139/apnm-2013-0084
Power KE, Lockyer EJ, Forman DA, Button DC (2018) Modulation of motoneurone excitability during rhythmic motor outputs. Appl Physiol Nutr Metab 43:1176–1185. https://doi.org/10.1139/apnm-2018-0077
doi: 10.1139/apnm-2018-0077
pubmed: 29522692
Roeleveld K, Stegeman DF, Vingerhoets HM, Van Oosterom A (1997) The motor unit potential distribution over the skin surface and its use in estimating the motor unit location. Acta Physiol Scand 161:465–472. https://doi.org/10.1046/j.1365-201X.1997.00247.x
doi: 10.1046/j.1365-201X.1997.00247.x
pubmed: 9429653
Schmidt BJ (1994) Afterhyperpolarization modulation in lumbar motoneurons during locomotor-like rhythmic activity in the neonatal rat spinal cord in vitro. Exp Brain Res. https://doi.org/10.1007/BF00239588
doi: 10.1007/BF00239588
pubmed: 7957731
Sidhu SK, Cresswell AG, Carroll TJ (2012) Motor cortex excitability does not increase during sustained cycling exercise to volitional exhaustion. J Appl Physiol 113:401–409. https://doi.org/10.1152/japplphysiol.00486.2012
doi: 10.1152/japplphysiol.00486.2012
pubmed: 22678968
Stashuk D (2001) EMG signal decomposition: how can it be accomplished and used? J Electromyogr Kinesiol 11:151–173. https://doi.org/10.1016/S1050-6411(00)00050-X
doi: 10.1016/S1050-6411(00)00050-X
pubmed: 11335147
Tax AAM, van der Gon JJD, Gielen CCAM, van den Tempel CMM (1989) Differences in the activation of m. biceps brachii in the control of slow isotonic movements and isometric contractions. Exp Brain Res 76:55–63. https://doi.org/10.1007/BF00253623
doi: 10.1007/BF00253623
pubmed: 2753109
Thomas CK, Ross BH, Calancie B (1987) Human motor-unit recruitment during isometric contractions and repeated dynamic movements. J Neurophysiol 57:311–324. https://doi.org/10.1152/jn.1987.57.1.311
doi: 10.1152/jn.1987.57.1.311
pubmed: 3559678
Timmons JA (2011) Variability in training-induced skeletal muscle adaptation. J Appl Physiol 110:846–853. https://doi.org/10.1152/japplphysiol.00934.2010
doi: 10.1152/japplphysiol.00934.2010
pubmed: 21030666
Vieira TM, Botter A (2021) The accurate assessment of muscle excitation requires the detection of multiple surface electromyograms. Exerc Sport Sci Rev 49:23–34. https://doi.org/10.1249/JES.0000000000000240
doi: 10.1249/JES.0000000000000240
pubmed: 33044329
Vieira TMM, Loram ID, Muceli S et al (2011) Postural activation of the human medial gastrocnemius muscle: are the muscle units spatially localised? J Physiol London 589:431–443. https://doi.org/10.1113/jphysiol.2010.201806
doi: 10.1113/jphysiol.2010.201806
pubmed: 21115645
Vieira TM, Bisi MC, Stagni R, Botter A (2017a) Changes in tibialis anterior architecture affect the amplitude of surface electromyograms. J Neuroeng Rehabil 14:81. https://doi.org/10.1186/s12984-017-0291-5
doi: 10.1186/s12984-017-0291-5
pubmed: 28807025
pmcid: 5557318
Vieira TM, Bisi MC, Stagni R, Botter A (2017b) Changes in tibialis anterior architecture affect the amplitude of surface electromyograms. J Neuroeng Rehabil. https://doi.org/10.1186/s12984-017-0291-5
doi: 10.1186/s12984-017-0291-5
pubmed: 28807025
pmcid: 5557318
Vieira TM, Lemos T, Oliveira LAS et al (2019) Postural muscle unit plasticity in stroke survivors: altered distribution of gastrocnemius’ action potentials. Front Neurol 10:1–10. https://doi.org/10.3389/fneur.2019.00686
doi: 10.3389/fneur.2019.00686
Vila-Chã C, Falla D, Farina D (2010) Motor unit behavior during submaximal contractions following six weeks of either endurance or strength training. J Appl Physiol 109:1455–1466. https://doi.org/10.1152/japplphysiol.01213.2009
doi: 10.1152/japplphysiol.01213.2009
pubmed: 20829500
Wakahara T, Fukutani A, Kawakami Y, Yanai T (2013) Nonuniform muscle hypertrophy: its relation to muscle activation in training session. Med Sci Sports Exerc 45:2158–2165. https://doi.org/10.1249/MSS.0b013e3182995349
doi: 10.1249/MSS.0b013e3182995349
pubmed: 23657165
Woodrow L, Sheppard P, Gardiner PF (2013) Transcriptional changes in rat α-motoneurons resulting from increased physical activity. Neuroscience 255:45–54. https://doi.org/10.1016/j.neuroscience.2013.09.038
doi: 10.1016/j.neuroscience.2013.09.038
pubmed: 24080428
Yeo WK, Paton CD, Garnham AP et al (2008) Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens. J Appl Physiol 105:1462–1470. https://doi.org/10.1152/japplphysiol.90882.2008
doi: 10.1152/japplphysiol.90882.2008
pubmed: 18772325
Zehr EP, Duysens J (2004) Regulation of arm and leg movement during human locomotion. Neuroscientist 10:347–361. https://doi.org/10.1177/1073858404264680
doi: 10.1177/1073858404264680
pubmed: 15271262
Zehr EP, Carroll TJ, Chua R, Collins DF (2004) Possible contributions of CPG activity to the control of rhythmic human arm movement. Can J Physiol Pharmacol 82:13
doi: 10.1139/y04-056