Abstract
The purpose of this study was to investigate age-related differences in short-term training adaptations in cortical excitability and inhibition. Thirty young (21.9 ± 3.1 years) and 30 older (72.9 ± 4.6 years) individuals participated in the study. Each participant was randomly assigned to a control (n = 30) or a resistance training (n = 30) group, with equal numbers of young and older subjects in each group. Participants completed 2 days of testing, separated by 2 weeks during which time the training group participated in resistance training of the ankle dorsiflexor muscles three times per week. During each testing session, transcranial magnetic stimulation was used to generate motor evoked potentials (MEPs) and silent periods in the tibialis anterior. Hoffmann reflexes (H-reflexes) and compound muscle action potentials (M-waves) were also evoked via electrical stimulation of the peroneal nerve. At baseline, young subjects had higher maximum voluntary contraction (MVC) force (p = 0.002), larger M-wave amplitude (p < 0.001), and longer duration silent periods (p = 0.01) than older individuals, with no differences in the maximal amplitude of the MEP (p = 0.23) or H-reflex (p = 0.57). In the trained group, MVC increased in both young (17.4 %) and older (19.8 %) participants (p < 0.001), and the duration of the silent period decreased by ~15 and 12 ms, respectively (p < 0.001). Training did not significantly impact MEP (p = 0.69) or H-reflex amplitudes (p = 0.38). There were no significant changes in any measures in the control group (p ≥ 0.19) across the two testing sessions. These results indicate that a reduction in cortical inhibition may be an important neural adaptation in response to training in both young and older adults.
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References
Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P (2002) Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol 93:1318–1326. doi:10.1152/japplphysiol.00283.2002
Abbruzzese G, Assini A, Buccolieri A, Marchese R, Trompetto C (1999) Changes of intracortical inhibition during motor imagery in human subjects. Neurosci Lett 263:113–116
Andersson SA, Landgren S, Wolsk D (1966) The thalamic relay and cortical projection of group I muscle afferents from the forelimb of the cat. J Physiol 183:576–591
Brerro-Saby C, Delliaux S, Steinberg JG, Jammes Y (2008) Fatigue-induced changes in tonic vibration response (TVR) in humans: relationships between electromyographic and biochemical events. Muscle Nerve 38:1481–1489. doi:10.1002/mus.21117
Carroll TJ, Riek S, Carson RG (2002) The sites of neural adaptation induced by resistance training in humans. J Physiol 544:641–652
Carroll TJ, Riek S, Carson RG (2001) Reliability of the input–output properties of the cortico-spinal pathway obtained from transcranial magnetic and electrical stimulation. J Neurosci Methods 112:193–202
Christie A, Kamen G (2010) Short-term training adaptations in maximal motor unit firing rates and afterhyperpolarization duration. Muscle Nerve 41:651–660. doi:10.1002/mus.21539
Christie A, Lester S, LaPierre D, Gabriel DA (2004) Reliability of a new measure of H-reflex excitability. Clin Neurophysiol 115:116–123
Cirillo J, Todd G, Semmler JG (2011) Corticomotor excitability and plasticity following complex visuomotor training in young and old adults. Eur J Neurosci 34:1847–1856. doi:10.1111/j.1460-9568.2011.07870
De Beaumont L, Theoret H, Mongeon D, Messier J, Leclerc S, Tremblay S, Ellemberg D, Lassonde M (2009) Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 132:695–708. doi:10.1093/brain/awn347
Degtyarenko AM, Kaufman MP (2002) Spinoreticular neurons that receive group III input are inhibited by MLR stimulation. J Appl Physiol 93:92–98. doi:10.1152/japplphysiol.00072.2002
Devanne H, Lavoie BA, Capaday C (1997) Input–output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338
Eisen A, Entezari-Taher M, Stewart H (1996) Cortical projections to spinal motoneurons: changes with aging and amyotrophic lateral sclerosis. Neurology 46:1396–1404
Gandevia SC, Burke D (1990) Projection of thenar muscle afferents to frontal and parietal cortex of human subjects. Electroencephalogr Clin Neurophysiol 77:353–361
Gandevia SC, Burke D, McKeon B (1984) The projection of muscle afferents from the hand to cerebral cortex in man. Brain 107(Pt 1):1–13
Garland SJ, McComas AJ (1990) Reflex inhibition of human soleus muscle during fatigue. J Physiol 429:17–27
Garvey MA, Ziemann U, Becker DA, Barker CA, Bartko JJ (2001) New graphical method to measure silent periods evoked by transcranial magnetic stimulation. Clin Neurophysiol 112:1451–1460
Griffin L, Cafarelli E (2007) Transcranial magnetic stimulation during resistance training of the tibialis anterior muscle. J Electromyogr Kinesiol 17:446–452. doi:10.1016/j.jelekin.2006.05.001
Hortobagyi T, Devita P (2006) Mechanisms responsible for the age-associated increase in coactivation of antagonist muscles. Exerc Sport Sci Rev 34:29–35
Hunter GR, McCarthy JP, Bamman MM (2004) Effects of resistance training on older adults. Sports Med 34:329–348
Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 466:521–534
Kamen G (2005) Aging, resistance training, and motor unit discharge behavior. Can J Appl Physiol 30:341–351
Kamen G, Knight CA (2004) Training-related adaptations in motor unit discharge rate in young and older adults. J Gerontol A Biol Sci Med Sci 59:1334–1338
Kamen G, Sison SV, Du CC, Patten C (1995) Motor unit discharge behavior in older adults during maximal-effort contractions. J Appl Physiol 79:1908–1913
Kidgell DJ, Pearce AJ (2010) Corticospinal properties following short-term strength training of an intrinsic hand muscle. Hum Mov Sci 29:631–641. doi:10.1016/j.humov.2010.01.004
Knight CA, Kamen G (2001) Adaptations in muscular activation of the knee extensor muscles with strength training in young and older adults. J Electromyogr Kinesiol 11:405–412
Koceja DM, Mynark RG (2000) Comparison of heteronymous monosynaptic Ia facilitation in young and elderly subjects in supine and standing positions. Int J Neurosci 103:1–17
Kumru H, Soto O, Casanova J, Valls-Sole J (2008) Motor cortex excitability changes during imagery of simple reaction time. Exp Brain Res 189:373–378. doi:10.1007/s00221-008-1433-6
Ling LJ, Honda T, Shimada Y, Ozaki N, Shiraishi Y, Sugiura Y (2003) Central projection of unmyelinated (C) primary afferent fibers from gastrocnemius muscle in the guinea pig. J Comp Neurol 461:140–150. doi:10.1002/cne.10619
Macaluso A, De Vito G (2004) Muscle strength, power and adaptations to resistance training in older people. Eur J Appl Physiol 91:450–472. doi:10.1007/s00421-003-0991-3
McDonnell MN, Orekhov Y, Ziemann U (2007) Suppression of LTP-like plasticity in human motor cortex by the GABAB receptor agonist baclofen. Exp Brain Res 180:181–186. doi:10.1007/s00221-006-0849-0
McNeil CJ, Doherty TJ, Stashuk DW, Rice CL (2005) Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men. Muscle Nerve 31:461–467. doi:10.1002/mus.20276
Oliviero A, Profice P, Tonali PA, Pilato F, Saturno E, Dileone M, Ranieri F, Di Lazzaro V (2006) Effects of aging on motor cortex excitability. Neurosci Res 55:74–77. doi:10.1016/j.neures.2006.02.002
Patten C, Kamen G, Rowland DM (2001) Adaptations in maximal motor unit discharge rate to strength training in young and older adults. Muscle Nerve 24:542–550
Perez MA, Lungholt BK, Nyborg K, Nielsen JB (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res 159:197–205. doi:10.1007/s00221-004-1947-5
Pitcher JB, Ogston KM, Miles TS (2003) Age and sex differences in human motor cortex input–output characteristics. J Physiol 546:605–613
Rogasch NC, Dartnall TJ, Cirillo J, Nordstrom MA, Semmler JG (2009) Corticomotor plasticity and learning of a ballistic thumb training task are diminished in older adults. J Appl Physiol 107:1874–1883. doi:10.1152/japplphysiol.00443.2009
Rossini PM, Rossini L, Ferreri F (2010) Brain-behavior relations. IEEE Eng Med Biol 29:84-96. doi:10.1109/MEMB.2009.935474
Sale DG (1988) Neural adaptation to resistance training. Med Sci Sports Exerc 20:S135–45
Sale MV, Semmler JG (2005) Age-related differences in corticospinal control during functional isometric contractions in left and right hands. J Appl Physiol 99:1483–1493. doi:10.1152/japplphysiol.00371.2005
Stinear CM, Byblow WD (2004) Modulation of corticospinal excitability and intracortical inhibition during motor imagery is task-dependent. Exp Brain Res 157:351–358. doi:10.1007/s00221-004-1851-z
Terao Y, Ugawa Y (2002) Basic mechanisms of TMS. J Clin Neurophysiol 19:322–343
Vie B, Gomez N, Brerro-Saby C, Weber JP, Jammes Y (2013) Changes in stationary upright standing and proprioceptive reflex control of foot muscles after fatiguing static foot inversion. J Biomech 46:1676–1682. doi:10.1016/j.jbiomech.2013.04.005
Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J (1999) Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 517(Pt 2):591–597
Woods JJ, Furbush F, Bigland-Ritchie B (1987) Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. J Neurophysiol 58:125–137
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This work was partially funded by a grant from the American College of Sports Medicine (AD Christie).
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Christie, A., Kamen, G. Cortical inhibition is reduced following short-term training in young and older adults. AGE 36, 749–758 (2014). https://doi.org/10.1007/s11357-013-9577-0
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DOI: https://doi.org/10.1007/s11357-013-9577-0