Determining the early corticospinal-motoneuronal responses to strength training: a systematic review and meta-analysis

References

Borenstein, M., Hedges, V., and Larry, P.T. (2010). A basic introduction to fixed-effect and random effects models for meta-analysis. Res. Synth. Meth. 1, 97–111.10.1002/jrsm.12Search in Google Scholar PubMed

Brandner, C.R., Warmington, S.A., and Kidgell, D.J. (2015). Corticomotor excitability is increased following an acute bout of blood flow restriction resistance exercise. Fron. Hum. Neurosci. 9, 652.10.3389/fnhum.2015.00652Search in Google Scholar PubMed PubMed Central

Bunday, K.L. and Monica, P.A. (2012). Motor recovery after spinal cord injury enhanced by strengthening corticospinal synaptic transmission. Curr. Biol. 22, 2355–2361.10.1016/j.cub.2012.10.046Search in Google Scholar PubMed PubMed Central

Butefisch, C.M., Davis, B.C., Wise, S.P., Sawaki, L., Kopylev, L., Classen, J., and Cohen, L.G. (2000). Mechanisms of use-dependent plasticity in the human motor cortex. P. Natl. Acad. Sci. USA 97, 3661–3665.10.1073/pnas.97.7.3661Search in Google Scholar PubMed PubMed Central

Carroll, T.J., Riek, S., and Carson, R.G. (2001). Corticospinal responses to motor training revealed by transcranial magnetic stimulation. Exerc. Sport Sci. Rev. 29, 54–59.10.1249/00003677-200104000-00003Search in Google Scholar PubMed

Carroll, T.J., Riek, S., and Carson, R.G. (2002). The sites of neural adaptation induced by resistance training in humans. J. Physiol. 544, 641–652.10.1113/jphysiol.2002.024463Search in Google Scholar PubMed PubMed Central

Carroll, T.J., Lee, M., Hsu, M., and Sayde, J. (2008). Unilateral practice of a ballistic movement causes bilateral increases in performance and corticospinal excitability. J. Appl. Physiol. 104, 1656–1664.10.1152/japplphysiol.01351.2007Search in Google Scholar PubMed

Chen, R., Lozano, A.M., and Ashby, P. (1999). Mechanism of the silent period following transcranial magnetic stimulation. Evidence from epidural recordings. Exp. Br. Res. 128, 539–542.10.1007/s002210050878Search in Google Scholar PubMed

Christie, A. and Kamen, G. (2013). Cortical inhibition is reduced following short-term training in young and older adults. AGE. 36, 749–758.10.1007/s11357-013-9577-0Search in Google Scholar PubMed PubMed Central

Cirillo, J., Todd, G., and Semmler, J.G. (2011). Corticomotor excitability and plasticity following complex visuomotor training in young and old adults. Euro. J. Neurosci. 34, 1847–1856.10.1111/j.1460-9568.2011.07870.xSearch in Google Scholar PubMed

Clark, B.C., Issac, L.A., Lane, J.L., Damron, V., and Hoffman, R.A. (2008). Neuromuscular plasticity during and following 3 wk of human forearm cast immobilization. J. Appl. Physiol. 105, 868–878.10.1152/japplphysiol.90530.2008Search in Google Scholar PubMed

Clark, B.C., Taylor, J.L., Hoffman, R.L., Dearth, D.J., and Thomas, S.J. (2010). Cast immobilization increases long-interval intracortical inhibition. Muscle Nerve. 42, 363–372.10.1002/mus.21694Search in Google Scholar PubMed PubMed Central

Clark, B.C., Mahato, N.K., Nakazawa, M., Law, T.D., and Thomas, J.S. (2014). The power of the mind: the cortex as a critical determinant of muscle strength/weakness. J. Neurophysiol. 112, 3219–3226.10.1152/jn.00386.2014Search in Google Scholar PubMed PubMed Central

Coco, M., Alagona, G., Rapisarda, G., Costanzo, E., Calogero, R.A., and Perciavalle, V. (2010). Elevated blood lactate is associated with increased motor cortex excitability. Somatosens Mot. Res. 27, 1–8.10.3109/08990220903471765Search in Google Scholar PubMed

Cohen, J. (1988). Statistical Power for the Behavioral Sciences (Hillsdale: Lawrence Elbraum Associates).Search in Google Scholar

Coombs, T.A., Frazer, A.K., Horvath, D.M., Pearce, A.J., Howatson, G., and Kidgell, D.J. (2016). Cross-education of wrist extensor strength is not influenced by non-dominant training in right-handers. Euro. Apply. Physiol. 116, 1757–1769.10.1007/s00421-016-3436-5Search in Google Scholar PubMed

Dayan, E. and Cohen, L.G. (2011). Neuroplasticity subserving motor skill learning. Neuron 72, 443–454.10.1016/j.neuron.2011.10.008Search in Google Scholar PubMed PubMed Central

Di Lazzaro, V. and Ziemann, U. (2013). The contribution of transcranial magnetic stimulation in the functional evaluation of microcircuits in human motor cortex. Front. Neural Circuits 7, 18.10.3389/fncir.2013.00018Search in Google Scholar PubMed PubMed Central

Di Lazzaro, V., Restuccia, D., Oliviero, A., Profice, P., Ferrara, L., Insola, A., Mazzone, P., Tonali, P., and Rothwell, J.C. (1998). Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J. Physiol. 508, 625–633.10.1111/j.1469-7793.1998.625bq.xSearch in Google Scholar PubMed PubMed Central

Downs, S.H. and Black, N. (1998). The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J. Epi. Comm. Health 52, 377.10.1136/jech.52.6.377Search in Google Scholar PubMed PubMed Central

Enoka, R.M. (1988). Muscle strength and its development. New perspectives. Sports Med. 6, 146–168.10.2165/00007256-198806030-00003Search in Google Scholar PubMed

Frazer, A.K., Williams, J., Spittle, M., and Kidgell, D.J. (2017). Cross-education of muscular strength is facilitated by homeostatic plasticity. Euro. Appl. Physiol. 117, 665–677.10.1007/s00421-017-3538-8Search in Google Scholar PubMed

Goodall, S., Howatson, G., Thomas, K. (2018). Modulation of specific inhibitory networks in fatigued locomotor muscles of healthy males. Exp. Br. Res. 236, 463–473.10.1007/s00221-017-5142-xSearch in Google Scholar PubMed PubMed Central

Griffin, L. and Cafarelli, E. (2007). Transcranial magnetic stimulation during resistance training of the tibialis anterior muscle. J. Electromyogr. Kinesiol. 17, 446–452.10.1016/j.jelekin.2006.05.001Search in Google Scholar PubMed

Hendy, A.M. and Kidgell, D.J. (2013). Anodal tDCS applied during strength training enhances motor cortical plasticity. Med. Sci. Sport Exerc. 45, 1721–1729.10.1249/MSS.0b013e31828d2923Search in Google Scholar PubMed

Hendy, A.M. and Kidgell, D.J. (2014). Anodal-tDCS applied during unilateral strength training increases strength and corticospinal excitability in the untrained homologous muscle. Exp. Br. Res. 232, 3243–3252.10.1007/s00221-014-4016-8Search in Google Scholar PubMed

Higgins, J.P., Altman, D.G., Gøtzsche, P.C., Jüni, P., Moher, D., Oxman, A.D., Savovic, J., Schulz, K.F., Weeks, L., Sterne, J.A., et al. (2011). The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. Brit. Med. J. 343, d5928.10.1136/bmj.d5928Search in Google Scholar PubMed PubMed Central

Hortobágyi, T., Richardson, S.P., Lomarev, M., Shamim, E., Meunier, S., Russman, H., Dang, N., and Hallett, M. (2009). Chronic low-frequency rTMS of primary motor cortex diminishes exercise training-induced gains in maximal voluntary force in humans. J. Appl. Physiol. 106, 403–411.10.1152/japplphysiol.90701.2008Search in Google Scholar PubMed PubMed Central

Joseph, A. (2011). Plot Digitizer 2.5.1. Available from http://plotdigitizer.sourceforge.net/. Accessed date: 7, 2018.Search in Google Scholar

Katiuscia, S., Franco, C., Federico, D.A., Davide, M., Sergio, D., and Giuliano, G. (2009). Reorganization and enhanced functional connectivity of motor areas in repetitive ankle movements after training in locomotor attention. Brain Res. 1297, 124–134.10.1016/j.brainres.2009.08.049Search in Google Scholar PubMed

Kidgell, D.J., Stokes, M.A., Castricum, T.J., and Pearce, A.J. (2010). Neurophysiological responses after short-term strength training of the biceps brachii muscle. J. Strength Cond. Res. 24, 3123–3132.10.1519/JSC.0b013e3181f56794Search in Google Scholar PubMed

Kidgell, D.J., Bonanno, D.R., Frazer, A.K., Howatson, G., and Pearce, A.J. (2017). Corticospinal responses following strength training: a systematic review and meta-analysis. Euro. J. Neurosci. 46, 2648–2661.10.1111/ejn.13710Search in Google Scholar PubMed

Kleim, J.A., Barbay, S., Cooper, N.R., Hogg, T.M., Reidel, C.N., Remple, M.S., and Nudo, R.J. (2002). Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol. Learn Mem. 77, 63–77.10.1006/nlme.2000.4004Search in Google Scholar PubMed

Kujirai, T., Caramia, M.D., Rothwell, J.C., Day, B.L., Thompson, P.D., Ferbert, A., Wroe, S., Asselman, P., and Marsden, C.D. (1993). Corticocortical inhibition in human motor cortex. J. Physiol. 471, 501–519.10.1113/jphysiol.1993.sp019912Search in Google Scholar PubMed PubMed Central

Latella, C., Kidgell, D.J., and Pearce, A.J. (2012). Reduction in corticospinal inhibition in the trained and untrained limb following unilateral leg strength training. Eur. J. Appl. Physiol. 112, 3097–3107.10.1007/s00421-011-2289-1Search in Google Scholar PubMed

Latella, C., Hendy, A.M., Pearce, A.J., Vanderwesthuizen, D., and Teo, W.-P. (2016). The time-course of acute changes in corticospinal excitability, intra-cortical inhibition and facilitation following a single-session heavy strength training of the biceps brachii. Front. Hum. Neurosci. 10, 607. doi:10.1007/s00421-017-3709-7.10.3389/fnhum.2016.00607Search in Google Scholar PubMed PubMed Central

Latella, C., Teo, W.-P., Harris, D., Major, B., VanderWesthuizen, D., and Hendy, A.M. (2017). Effects of acute resistance training modality on corticospinal excitability, intra-cortical and neuromuscular responses. Eur. J. Appl. Physiol. 117, 2211–2224.10.1007/s00421-017-3709-7Search in Google Scholar PubMed

Latella, C., Hendy, A.M., Vanderwesthuizen, D., and Teo, W.P. (2018). The modulation of corticospinal excitability and inhibition following acute resistance exercise in males and females. Eur. J. Sport Sci. 18, 984–993.10.1080/17461391.2018.1467489Search in Google Scholar PubMed

Legrand, D., Vaes, B., Matheï, C., Adriaensen, W., Van Pottelbergh, G., and Degryse, J.M. (2014). Muscle strength and physical performance as predictors of mortality, hospitalization, and disability in the oldest old. J. Am. Geri. Soc. 62, 1030–1038.10.1111/jgs.12840Search in Google Scholar PubMed

Leung, M., Rantalainen, T., Teo, W.P., and Kidgell, D.J. (2015). Motor cortex excitability is not differentially modulated following skill and strength training. Neuroscience 305, 99–108.10.1016/j.neuroscience.2015.08.007Search in Google Scholar PubMed

Leung, M., Rantalainen, T., Teo, W.P., and Kidgell, D.J. (2017). The corticospinal responses of metronome-paced, but not self-paced strength training are similar to motor skill training. Eur. J. Appl. Physiol. 117, 2479–2492.10.1007/s00421-017-3736-4Search in Google Scholar PubMed

Liberati, A., Altman, D.G., Tetzlaff, J., Mulrow, C., Gøtzsche, P.C., Ioannidis, J.P.A., Clarke, M., Devereaux, P.J., Kleijnen, J., and Moher, D. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 6, e1000100.10.1371/journal.pmed.1000100Search in Google Scholar PubMed PubMed Central

Manca, A., Ginatempo, F., Cabboi, M.P., Mercante, B., Ortu, E., Dragone, D., De Natale, E.R., Dvir, Z., Rothwell, J.C., and Deriu, F. (2016). No evidence of neural adaptations following chronic unilateral isometric training of the intrinsic muscles of the hand: a randomized controlled study. Eur. J. Appl. Physiol. 116, 1993–2005.10.1007/s00421-016-3451-6Search in Google Scholar PubMed

Manca, A., Hortobagyi, T., Rothwell, J.C., and Deriu, F. (2018). Neurophysiological adaptations in theuntrained side in conjunction with cross-education of muscle strength: a systematic review and meta-analysis. J. Appl. Physiol. 124, 1502–1518.10.1152/japplphysiol.01016.2017Search in Google Scholar PubMed

Mason, J., Frazer, A.K., Horvath, D.M., Pearce, A.J., Avela, J., Howatson, G., and Kidgell, D.J. (2017). Adaptations in corticospinal excitability and inhibition are not spatially confined to the agonist muscle following strength training. Eur. J. Appl. Physio. 117, 1359–1371.10.1007/s00421-017-3624-ySearch in Google Scholar PubMed

Mazzocchio, R., Rothwell, J.C., Day, B.L., and Thompson, P.D. (1994). Effect of tonic voluntary activity on the excitability of human motor cortex. J. Physiol. 472, 261–267.10.1113/jphysiol.1994.sp020018Search in Google Scholar PubMed PubMed Central

McDonnell, M., Orekhov, Y., and Ziemann, U. (2006). The role of GABA_B receptors in intracortical inhibition in the human motor cortex. Exp. Br. Res. 173, 86–93.10.1007/s00221-006-0365-2Search in Google Scholar PubMed

Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann. Internal Medicine 151, 264–269.10.7326/0003-4819-151-4-200908180-00135Search in Google Scholar PubMed

Moreland, J.D., Richardson, A.J., Goldsmith, C.H., and Clase, C.M. (2004). Muscle weakness and falls in older adults: a systematic review and meta-analysis. J. Am. Geris. Soc. 52, 1121–1129.10.1111/j.1532-5415.2004.52310.xSearch in Google Scholar PubMed

Muellbacher, W., Ziemann, U., Wissel, J., Dang, N., Kofler, M., Facchini, S., Boroojerdi, B., Poewe, W., and Hallett, M. (2002). Early consolidation in human primary motor cortex. Nature 415, 640–644.10.1038/nature712Search in Google Scholar PubMed

Nielsen, J. and Petersen, N. (1995). Changes in the effect of magnetic brain stimulation accompanying voluntary dynamic contraction in man. J. Physiol. 484, 777–789.10.1113/jphysiol.1995.sp020703Search in Google Scholar PubMed PubMed Central

Nuzzo, J.L., Barry, B.K., Gandevia, S.C., and Taylor, J.L. (2016). Acute strength training increases responses to stimulation of corticospinal axons. Med. Sci. Sports Exerc. 48, 139–150.10.1249/MSS.0000000000000733Search in Google Scholar PubMed

Rogasch, N.C., Daskalakis, Z.J., and Fitzgerald, P.B. (2014). Cortical inhibition, excitation, and connectivity in schizophrenia: a review of insights from transcranial magnetic stimulation. Schizo. Bull. 40, 685–696.10.1093/schbul/sbt078Search in Google Scholar

Ruotsalainen, I., Ahtiainen, J., Kidgell, D.J., and Avela, J. (2014). Changes in corticospinal excitability during an acute bout of resistance exercise in the elbow flexors. Eur. J. Appl. Physiol. 114, 1545–1553.10.1007/s00421-014-2884-zSearch in Google Scholar PubMed

Sanes, J.N. and Donoghue, J.P. (2000). Plasticity and primary motor cortex. Annu. Rev. Neurosci. 23, 393–415.10.1146/annurev.neuro.23.1.393Search in Google Scholar PubMed

Selvanayagam, V.S., Riek, S., and Carroll, T.J. (2011). Early neural responses to strength training. J. Appl. Physiol. 111, 367–375.10.1152/japplphysiol.00064.2011Search in Google Scholar PubMed

Spink, M.J., Fotoohabadi, M.R., Wee, E., Hill, K.D., Lord, S.R., and Menz, H.B. (2011). Foot and ankle strength, range of motion, posture, and deformity are associated with balance and functional ability in older adults. Arch. Phys. Med. Rehabil. 92, 68–75.10.1016/j.apmr.2010.09.024Search in Google Scholar PubMed

Suzuki, T., Bean, J.F., and Roger, F.A. (2002). Muscle power of the ankle flexors predicts functional performance in community-dwelling older women. J. Am. Geri. Soc. 49, 1161–1167.10.1046/j.1532-5415.2001.49232.xSearch in Google Scholar

Taylor, J.L. (2006). Stimulation at the cervicomedullary junction in human subjects. J. Electromyogr. Kinesiol. 16, 215–223.10.1016/j.jelekin.2005.07.001Search in Google Scholar PubMed

Taylor, J.L. and Gandevia, S.C. (2004). Noninvasive stimulation of the human corticospinal tract. J. Appl. Physiol. 96, 1496–1503.10.1152/japplphysiol.01116.2003Search in Google Scholar PubMed

Taylor, J.L. and Martin, P.G. (2009). Voluntary motor output is altered by spike-yiming-dependent changes in the human corticospinal pathway. J. Neurosci. 29, 11708.10.1523/JNEUROSCI.2217-09.2009Search in Google Scholar PubMed

Ugawa, Y., Terao, Y., Hanajima, R., Sakai, K., and Kanazawa, I. (1995). Facilitatory effect of tonic voluntary contraction on responses to motor cortex stimulation. Electroenceph. Clin. Neurophysiol. 97, 451–454.10.1016/0924-980X(95)00214-6Search in Google Scholar

Weier, A.T., Pearce, A.J., and Kidgell, D.J. (2012). Strength training reduces intracortical inhibition. Acta Physiol. 206, 109–119.10.1111/j.1748-1716.2012.02454.xSearch in Google Scholar

Wilson, S.A., Lockwood, R.J., Thickbroom, G.W., and Mastaglia, F.L. (1993). The muscle silent period following transcranial magnetic cortical stimulation. J. Neurol. Sci. 114, 216–222.10.1016/0022-510X(93)90301-ESearch in Google Scholar PubMed