Test-Retest Reliability of Homeostatic Plasticity in the Human Primary Motor Cortex

Tribikram Thapa, Siobhan M Schabrun, Tribikram Thapa, Siobhan M Schabrun

Abstract

Homeostatic plasticity regulates synaptic activity by preventing uncontrolled increases (long-term potentiation) or decreases (long-term depression) in synaptic efficacy. Homeostatic plasticity can be induced and assessed in the human primary motor cortex (M1) using noninvasive brain stimulation. However, the reliability of this methodology has not been investigated. Here, we examined the test-retest reliability of homeostatic plasticity induced and assessed in M1 using noninvasive brain stimulation in ten, right-handed, healthy volunteers on days 0, 2, 7, and 14. Homeostatic plasticity was induced in the left M1 using two blocks of anodal transcranial direct current stimulation (tDCS) applied for 7 min and 5 min, separated by a 3 min interval. To assess homeostatic plasticity, 15 motor-evoked potentials to single-pulse transcranial magnetic stimulation were recorded at baseline, between the two blocks of anodal tDCS, and at 0 min, 10 min, and 20 min follow-up. Test-retest reliability was evaluated using intraclass correlation coefficients (ICCs). Moderate-to-good test-retest reliability was observed for the M1 homeostatic plasticity response at all follow-up time points (0 min, 10 min, and 20 min, ICC range: 0.43-0.67) at intervals up to 2 weeks. The greatest reliability was observed when the homeostatic response was assessed at 10 min follow-up (ICC > 0.61). These data suggest that M1 homeostatic plasticity can be reliably induced and assessed in healthy individuals using two blocks of anodal tDCS at intervals of 48 hours, 7 days, and 2 weeks.

Figures

Figure 1
Figure 1
Experimental protocol for days 0, 2, 7, and 14. The corticomotor excitability was assessed at the beginning of each test session using 15 motor-evoked potentials (MEPs) recorded at 120% of resting motor threshold. To ensure a consistent level of baseline corticomotor excitability across subjects prior to the induction of plasticity, further 15 MEPs were recorded at an intensity sufficient to elicit an average MEP of 1 mV peak-to-peak amplitude (S1mV) immediately before the first block of 7 min anodal transcranial direct current stimulation (tDCS). This intensity was kept consistent for the remainder of the test session. Plasticity was induced using a 7 min block of anodal tDCS, followed by a second 5 min block of anodal tDCS, separated by a 3 min rest period. Fifteen MEPs were recorded at S1mV between the two blocks of anodal tDCS, and at 0 min, 10 min, and 20 min follow-ups.
Figure 2
Figure 2
Group data (mean + SD) for motor-evoked potential (MEP) amplitude before the double tDCS protocol (“baseline”), after the first block of anodal tDCS (“between”), and at 0 min, 10 min, and 20 min follow-ups on days 0, 2, 7, and 14.

References

    1. Ziemann U., Siebner H. R. Modifying motor learning through gating and homeostatic metaplasticity. Brain Stimulation. 2008;1(1):60–66. doi: 10.1016/j.brs.2007.08.003.
    1. Bear M. F. Bidirectional synaptic plasticity: from theory to reality. Philosophical Transactions of the Royal Society B: Biological Sciences. 2003;358(1432):649–655. doi: 10.1098/rstb.2002.1255.
    1. Karabanov A., Ziemann U., Hamada M., et al. Consensus paper: probing homeostatic plasticity of human cortex with non-invasive transcranial brain stimulation. Brain Stimulation. 2015;8(3):442–454. doi: 10.1016/j.brs.2015.01.404.
    1. Muller-Dahlhaus F., Ziemann U. Metaplasticity in human cortex. The Neuroscientist. 2015;21(2):185–202. doi: 10.1177/1073858414526645.
    1. Turrigiano G. Homeostatic signaling: the positive side of negative feedback. Current Opinion in Neurobiology. 2007;17(3):318–324. doi: 10.1016/j.conb.2007.04.004.
    1. Turrigiano G. G. Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends in Neurosciences. 1999;22(5):221–227. doi: 10.1016/S0166-2236(98)01341-1.
    1. Gisabella B., Rowan M. J., Anwyl R. Mechanisms underlying the inhibition of long-term potentiation by preconditioning stimulation in the hippocampus in vitro. Neuroscience. 2003;121(2):297–305. doi: 10.1016/S0306-4522(03)00440-8.
    1. Huang Y. Y., Colino A., Selig D. K., Malenka R. C. The influence of prior synaptic activity on the induction of long-term potentiation. Science. 1992;255(5045):730–733. doi: 10.1126/science.1346729.
    1. Fricke K., Seeber A. A., Thirugnanasambandam N., Paulus W., Nitsche M. A., Rothwell J. C. Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. Journal of Neurophysiology. 2011;105(3):1141–1149. doi: 10.1152/jn.00608.2009.
    1. Siebner H. R., Lang N., Rizzo V., et al. Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. The Journal of Neuroscience. 2004;24(13):3379–3385. doi: 10.1523/JNEUROSCI.5316-03.2004.
    1. Antal A., Lang N., Boros K., Nitsche M., Siebner H. R., Paulus W. Homeostatic metaplasticity of the motor cortex is altered during headache-free intervals in migraine with aura. Cerebral Cortex. 2008;18(11):2701–2705. doi: 10.1093/cercor/bhn032.
    1. Cosentino G., Fierro B., Vigneri S., et al. Cyclical changes of cortical excitability and metaplasticity in migraine: evidence from a repetitive transcranial magnetic stimulation study. Pain. 2014;155(6):1070–1078. doi: 10.1016/j.pain.2014.02.024.
    1. Kang J. S., Terranova C., Hilker R., Quartarone A., Ziemann U. Deficient homeostatic regulation of practice-dependent plasticity in writer’s cramp. Cerebral Cortex. 2011;21(5):1203–1212. doi: 10.1093/cercor/bhq204.
    1. Thapa T., Graven-Nielsen T., Chipchase L. S., Schabrun S. M. Disruption of cortical synaptic homeostasis in individuals with chronic low back pain. Clinical Neurophysiology. 2018;129(5):1090–1096. doi: 10.1016/j.clinph.2018.01.060.
    1. Quartarone A., Rizzo V., Bagnato S., et al. Homeostatic-like plasticity of the primary motor hand area is impaired in focal hand dystonia. Brain. 2005;128(8):1943–1950. doi: 10.1093/brain/awh527.
    1. Brighina F., Giglia G., Scalia S., Francolini M., Palermo A., Fierro B. Facilitatory effects of 1 Hz rTMS in motor cortex of patients affected by migraine with aura. Experimental Brain Research. 2005;161(1):34–38. doi: 10.1007/s00221-004-2042-7.
    1. Brighina F., Piazza A., Daniele O., Fierro B. Modulation of visual cortical excitability in migraine with aura: effects of 1 Hz repetitive transcranial magnetic stimulation. Experimental Brain Research. 2002;145(2):177–181. doi: 10.1007/s00221-002-1096-7.
    1. Oldfield R. C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113. doi: 10.1016/0028-3932(71)90067-4.
    1. Keel J. C., Smith M. J., Wassermann E. M. A safety screening questionnaire for transcranial magnetic stimulation. Clinical Neurophysiology. 2001;112(4):p. 720. doi: 10.1016/S1388-2457(00)00518-6.
    1. Uy J., Ridding M. C., Miles T. S. Stability of maps of human motor cortex made with transcranial magnetic stimulation. Brain Topography. 2002;14(4):293–297. doi: 10.1023/A:1015752711146.
    1. Bastani A., Jaberzadeh S. A higher number of TMS-elicited MEP from a combined hotspot improves intra- and inter-session reliability of the upper limb muscles in healthy individuals. PLoS One. 2012;7(10, article e47582) doi: 10.1371/journal.pone.0047582.
    1. Chang W. H., Fried P. J., Saxena S., et al. Optimal number of pulses as outcome measures of neuronavigated transcranial magnetic stimulation. Clinical Neurophysiology. 2016;127(8):2892–2897. doi: 10.1016/j.clinph.2016.04.001.
    1. Christie A., Fling B., Crews R. T., Mulwitz L. A., Kamen G. Reliability of motor-evoked potentials in the ADM muscle of older adults. Journal of Neuroscience Methods. 2007;164(2):320–324. doi: 10.1016/j.jneumeth.2007.05.011.
    1. Doeltgen S. H., Ridding M. C., O’Beirne G. A., Dalrymple-Alford J., Huckabee M. L. Test–retest reliability of motor evoked potentials (MEPs) at the submental muscle group during volitional swallowing. Journal of Neuroscience Methods. 2009;178(1):134–137. doi: 10.1016/j.jneumeth.2008.12.005.
    1. Groppa S., Oliviero A., Eisen A., et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clinical Neurophysiology. 2012;123(5):858–882. doi: 10.1016/j.clinph.2012.01.010.
    1. Rossini P. M., Barker A. T., Berardelli A., et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalography and Clinical Neurophysiology. 1994;91(2):79–92. doi: 10.1016/0013-4694(94)90029-9.
    1. Nitsche M. A., Cohen L. G., Wassermann E. M., et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimulation. 2008;1(3):206–223. doi: 10.1016/j.brs.2008.06.004.
    1. Richardson J. T. E. Eta squared and partial eta squared as measures of effect size in educational research. Educational Research Review. 2011;6(2):135–147. doi: 10.1016/j.edurev.2010.12.001.
    1. Cohen J. Statistical Power Analysis for the Behavioural Sciences. New York, NY, USA: Academic Press; 1969.
    1. Schambra H. M., Ogden R. T., Martinez-Hernandez I. E., et al. The reliability of repeated TMS measures in older adults and in patients with subacute and chronic stroke. Frontiers in Cellular Neuroscience. 2015;9:p. 335. doi: 10.3389/fncel.2015.00335.
    1. McGraw K. O., Wong S. P. Forming inferences about some intraclass correlation coefficients. Psychological Methods. 1996;1(1):30–46. doi: 10.1037/1082-989X.1.1.30.
    1. Matamala J. M., Howells J., Dharmadasa T., et al. Inter-session reliability of short-interval intracortical inhibition measured by threshold tracking TMS. Neuroscience Letters. 2018;674:18–23. doi: 10.1016/j.neulet.2018.02.065.
    1. Turrigiano G. G., Nelson S. B. Homeostatic plasticity in the developing nervous system. Nature Reviews Neuroscience. 2004;5(2):97–107. doi: 10.1038/nrn1327.
    1. Abraham W. C. Metaplasticity: tuning synapses and networks for plasticity. Nature Reviews Neuroscience. 2008;9(5):p. 387. doi: 10.1038/nrn2356.
    1. Turrigiano G. Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harbor Perspectives in Biology. 2012;4(1, article a005736) doi: 10.1101/cshperspect.a005736.
    1. Karabanov A., Siebner H. R. Unravelling homeostatic interactions in inhibitory and excitatory networks in human motor cortex. The Journal of Physiology. 2012;590(22):5557–5558. doi: 10.1113/jphysiol.2012.244749.
    1. Lang N., Siebner H. R., Ernst D., et al. Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction of after-effects. Biological Psychiatry. 2004;56(9):634–639. doi: 10.1016/j.biopsych.2004.07.017.
    1. Sidhu S. K., Pourmajidian M., Opie G. M., Semmler J. G. Increasing motor cortex plasticity with spaced paired associative stimulation at different intervals in older adults. European Journal of Neuroscience. 2017;46(11):2674–2683. doi: 10.1111/ejn.13729.
    1. Opie G. M., Vosnakis E., Ridding M. C., Ziemann U., Semmler J. G. Priming theta burst stimulation enhances motor cortex plasticity in young but not old adults. Brain Stimulation. 2017;10(2):298–304. doi: 10.1016/j.brs.2017.01.003.
    1. Fujiyama H., Hinder M. R., Barzideh A., et al. Preconditioning tDCS facilitates subsequent tDCS effect on skill acquisition in older adults. Neurobiology of Aging. 2017;51:31–42. doi: 10.1016/j.neurobiolaging.2016.11.012.
    1. Christova M., Rafolt D., Gallasch E. Cumulative effects of anodal and priming cathodal tDCS on pegboard test performance and motor cortical excitability. Behavioural Brain Research. 2015;287:27–33. doi: 10.1016/j.bbr.2015.03.028.
    1. Malcolm M. P., Triggs W. J., Light K. E., Shechtman O., Khandekar G., Gonzalez Rothi L. J. Reliability of motor cortex transcranial magnetic stimulation in four muscle representations. Clinical Neurophysiology. 2006;117(5):1037–1046. doi: 10.1016/j.clinph.2006.02.005.
    1. Liu H., Au-Yeung S. S. Y. Reliability of transcranial magnetic stimulation induced corticomotor excitability measurements for a hand muscle in healthy and chronic stroke subjects. Journal of the Neurological Sciences. 2014;341(1-2):105–109. doi: 10.1016/j.jns.2014.04.012.
    1. Brighina F., Cosentino G., Vigneri S., et al. Abnormal facilitatory mechanisms in motor cortex of migraine with aura. European Journal of Pain. 2011;15(9):928–935. doi: 10.1016/j.ejpain.2011.03.012.
    1. Jung P., Ziemann U. Homeostatic and nonhomeostatic modulation of learning in human motor cortex. The Journal of Neuroscience. 2009;29(17):5597–5604. doi: 10.1523/JNEUROSCI.0222-09.2009.
    1. Huang Y. Z., Rothwell J. C., Lu C. S., Chuang W. L., Chen R. S. Abnormal bidirectional plasticity-like effects in Parkinson’s disease. Brain. 2011;134(8):2312–2320. doi: 10.1093/brain/awr158.
    1. Goldsworthy M. R., Pitcher J. B., Ridding M. C. The application of spaced theta burst protocols induces long-lasting neuroplastic changes in the human motor cortex. European Journal of Neuroscience. 2012;35(1):125–134. doi: 10.1111/j.1460-9568.2011.07924.x.
    1. Goldsworthy M. R., Muller-Dahlhaus F., Ridding M. C., Ziemann U. Resistant against de-depression: LTD-like plasticity in the human motor cortex induced by spaced cTBS. Cerebral Cortex. 2015;25(7):1724–1734. doi: 10.1093/cercor/bht353.
    1. Nitsche M. A., Nitsche M. S., Klein C. C., Tergau F., Rothwell J. C., Paulus W. Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clinical Neurophysiology. 2003;114(4):600–604. doi: 10.1016/S1388-2457(02)00412-1.
    1. Nitsche M. A., Paulus W. Transcranial direct current stimulation—update 2011. Restorative Neurology and Neuroscience. 2011;29(6):463–492. doi: 10.3233/RNN-2011-0618.
    1. Biabani M., Aminitehrani M., Zoghi M., Farrell M., Egan G., Jaberzadeh S. The effects of transcranial direct current stimulation on short-interval intracortical inhibition and intracortical facilitation: a systematic review and meta-analysis. Reviews in the Neurosciences. 2017;29(1):99–114. doi: 10.1515/revneuro-2017-0023.
    1. Brighina F., Palermo A., Daniele O., Aloisio A., Fierro B. High-frequency transcranial magnetic stimulation on motor cortex of patients affected by migraine with aura: a way to restore normal cortical excitability? Cephalalgia. 2010;30(1):46–52. doi: 10.1111/j.1468-2982.2009.01870.x.
    1. Bastani A., Jaberzadeh S. a-tDCS differential modulation of corticospinal excitability: the effects of electrode size. Brain Stimulation. 2013;6(6):932–937. doi: 10.1016/j.brs.2013.04.005.
    1. DaSilva A. F., Volz M. S., Bikson M., Fregni F. Electrode positioning and montage in transcranial direct current stimulation. Journal of Visualized Experiments. 2011;51, article e2744 doi: 10.3791/2744.
    1. Bocci T., Caleo M., Tognazzi S., et al. Evidence for metaplasticity in the human visual cortex. Journal of Neural Transmission. 2014;121(3):221–231. doi: 10.1007/s00702-013-1104-z.
    1. Bliem B., Muller-Dahlhaus J. F., Dinse H. R., Ziemann U. Homeostatic metaplasticity in the human somatosensory cortex. Journal of Cognitive Neuroscience. 2008;20(8):1517–1528. doi: 10.1162/jocn.2008.20106.
    1. Wolters A., Schmidt A., Schramm A., et al. Timing-dependent plasticity in human primary somatosensory cortex. The Journal of Physiology. 2005;565(3):1039–1052. doi: 10.1113/jphysiol.2005.084954.
    1. Jones C. B., Lulic T., Bailey A. Z., et al. Metaplasticity in human primary somatosensory cortex: effects on physiology and tactile perception. Journal of Neurophysiology. 2016;115(5):2681–2691. doi: 10.1152/jn.00630.2015.

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