Interindividual variability and age-dependency of motor cortical plasticity induced by paired associative stimulation

Springer Science and Business Media LLC - Tập 187 - Trang 467-475 - 2008
J. Florian M. Müller-Dahlhaus1, Yuriy Orekhov1, Yali Liu1,2, Ulf Ziemann1
1Motor Cortex Group, Department of Neurology, Johann Wolfgang Goethe-University, Frankfurt am Main, Germany
2Department of Rehabilitation Medicine, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, People’s Republic of China

Tóm tắt

Paired associative stimulation (PAS) can increase motor cortical excitability, possibly by long-term potentiation (LTP)-like mechanisms. As the capability of the cortex for plasticity decreases with age, we were interested here in testing interindividual variability and age-dependency of the PAS effect. Motor-evoked potentials (MEPs) were recorded from the resting right abductor pollicis brevis muscle before and for 30 min after PAS in 27 healthy subjects (22–71 years of age). PAS consisted of 225 pairs (rate, 0.25 Hz) of right median nerve stimulation followed at an interval equaling the individual N20-latency of the median nerve somatosensory-evoked cortical potential plus 2 ms by transcranial magnetic stimulation of the hand area of left primary motor cortex (PASN20+2). The PASN20+2-induced changes in MEP amplitude (ratio post PAS/pre PAS) were highly variable (1.00 ± 0.07, range 0.36–1.68). Fourteen subjects showed the expected LTP-like MEP increase (responders) while 13 subjects showed a long-term depression (LTD)-like MEP decrease (non-responders). Responders had a significantly lower resting motor threshold (RMT) and minimum stimulus intensity to elicit MEPs of 1 mV (MEP1 mV) than non-responders. RMT and MEP1 mV correlated significantly negatively with the PASN20+2 effect. The absolute PASN20+2 effect size irrespective of its direction decreased with age (r = −0.57, P = 0.002), i.e., LTP-like and LTD-like plasticity were large in young subjects but substantially smaller in elderly subjects. In conclusion, measures of motor cortical excitability (RMT, MEP1 mV) and age determine direction and magnitude of PAS effects in individual subjects.

Tài liệu tham khảo

Adams I (1987) Plasticity of the synaptic contact zone following loss of synapses in the cerebral cortex of aging humans. Brain Res 424:343–351 Agnati LF, Zoli M, Grimaldi R, Fuxe K, Toffano G, Zini I (1990) Cellular and synaptic alterations in the aging brain. Aging (Milano) 2:5–25 Bagnato S, Agostino R, Modugno N, Quartarone A, Berardelli A (2006) Plasticity of the motor cortex in Parkinson’s disease patients on and off therapy. Mov Disord 21:639–645 Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39 Butefisch CM, Davis BC, Sawaki L, Waldvogel D, Classen J, Kopylev L, Cohen LG (2002) Modulation of use-dependent plasticity by d-amphetamine. Ann Neurol 51:59–68 Butefisch CM, Davis BC, Wise SP, Sawaki L, Kopylev L, Classen J, Cohen LG (2000) Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci USA 97:3661–3665 Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 129:1659–1673 Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P, Insola A, Tonali PA, Rothwell JC (2004) The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115:255–266 Earles D, Vardaxis V, Koceja D (2001) Regulation of motor output between young and elderly subjects. Clin Neurophysiol 112:1273–1279 Floel A, Breitenstein C, Hummel F, Celnik P, Gingert C, Sawaki L, Knecht S, Cohen LG (2005) Dopaminergic influences on formation of a motor memory. Ann Neurol 58:121–130 Fratello F, Veniero D, Curcio G, Ferrara M, Marzano C, Moroni F, Pellicciari MC, Bertini M, Rossini PM, De Gennaro L (2006) Modulation of corticospinal excitability by paired associative stimulation: reproducibility of effects and intraindividual reliability. Clin Neurophysiol 117:2667–2674 Gangitano M, Valero-Cabre A, Tormos JM, Mottaghy FM, Romero JR, Pascual-Leone A (2002) Modulation of input–output curves by low and high frequency repetitive transcranial magnetic stimulation of the motor cortex. Clin Neurophysiol 113:1249–1257 Hedden T, Gabrieli JD (2004) Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci 5:87–96 Jay TM (2003) Dopamine: a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol 69:375–390 Keel JC, Smith MJ, Wassermann EM (2001) A safety screening questionnaire for transcranial magnetic stimulation. Clin Neurophysiol 112:720 Kido A, Tanaka N, Stein RB (2004) Spinal excitation and inhibition decrease as humans age. Can J Physiol Pharmacol 82:238–248 Kleim JA, Chan S, Pringle E, Schallert K, Procaccio V, Jimenez R, Cramer SC (2006) BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex. Nat Neurosci 9:735–737 Kujirai K, Kujirai T, Sinkjaer T, Rothwell JC (2006) Associative plasticity in human motor cortex during voluntary muscle contraction. J Neurophysiol 96:1337–1346 Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 133:425–430 Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213–215 McDonnell MN, Orekhov Y, Ziemann U (2007) Suppression of LTP-like plasticity in human motor cortex by the GABA(B) receptor agonist baclofen. Exp Brain Res 180:181–186 Meintzschel F, Ziemann U (2006) Modification of practice-dependent plasticity in human motor cortex by neuromodulators. Cereb Cortex 16:1106–1115 Meunier SO, Russmann H, Simonetta-Moreau M, Hallett M (2007) Changes in spinal excitability after PAS (paired associative stimulation). J Neurophysiol (in press) Morgante F, Espay AJ, Gunraj C, Lang AE, Chen R (2006) Motor cortex plasticity in Parkinson’s disease and levodopa-induced dyskinesias. Brain 129:1059–1069 Morita H, Shindo M, Yanagawa S, Yoshida T, Momoi H, Yanagisawa N (1995) Progressive decrease in heteronymous monosynaptic Ia facilitation with human ageing. Exp Brain Res 104:167–170 Muller JF, Orekhov Y, Liu Y, Ziemann U (2007) Homeostatic plasticity in human motor cortex demonstrated by two consecutive sessions of paired associative stimulation. Eur J Neurosci 25:3461–3468 Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113 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 Peinemann A, Lehner C, Conrad B, Siebner HR (2001) Age-related decrease in paired-pulse intracortical inhibition in the human primary motor cortex. Neurosci Lett 313:33–36 Pitcher JB, Ogston KM, Miles TS (2003) Age and sex differences in human motor cortex input–output characteristics. J Physiol 546:605–613 Quartarone A, Bagnato S, Rizzo V, Siebner HR, Dattola V, Scalfari A, Morgante F, Battaglia F, Romano M, Girlanda P (2003) Abnormal associative plasticity of the human motor cortex in writer’s cramp. Brain 126:2586–2596 Quartarone A, Rizzo V, Bagnato S, Morgante F, Sant’angelo A, Girlanda P, Roman Siebner H (2006) Rapid-rate paired associative stimulation of the median nerve and motor cortex can produce long-lasting changes in motor cortical excitability in humans. J Physiol 575:657–670 Rioult-Pedotti MS, Friedman D, Donoghue JP (2000) Learning-induced LTP in neocortex. Science 290:533–536 Rioult-Pedotti MS, Friedman D, Hess G, Donoghue JP (1998) Strengthening of horizontal cortical connections following skill learning. Nat Neurosci 1:230–234 Romanczyk TB, Weickert CS, Webster MJ, Herman MM, Akil M, Kleinman JE (2002) Alterations in trkB mRNA in the human prefrontal cortex throughout the lifespan. Eur J Neurosci 15:269–280 Rosenkranz K, Rothwell JC (2006) Differences between the effects of three plasticity inducing protocols on the organization of the human motor cortex. Eur J Neurosci 23:822–829 Rosenkranz K, Williamon A, Rothwell JC (2007) Motorcortical excitability and synaptic plasticity is enhanced in professional musicians. J Neurosci 27:5200–5206 Sale MV, Ridding MC, Nordstrom MA (2007) Factors influencing the magnitude and reproducibility of corticomotor excitability changes induced by paired associative stimulation. Exp Brain Res 181(4):615–626 Sawaki L, Boroojerdi B, Kaelin-Lang A, Burstein AH, Butefisch CM, Kopylev L, Davis B, Cohen LG (2002) Cholinergic influences on use-dependent plasticity. J Neurophysiol 87:166–171 Sawaki L, Yaseen Z, Kopylev L, Cohen LG (2003) Age-dependent changes in the ability to encode a novel elementary motor memory. Ann Neurol 53:521–524 Stefan K, Kunesch E, Benecke R, Cohen LG, Classen J (2002) Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol 543:699–708 Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123 (Pt 3):572–584 Stefan K, Wycislo M, Classen J (2004) Modulation of associative human motor cortical plasticity by attention. J Neurophysiol 92:66–72 Stefan K, Wycislo M, Gentner R, Schramm A, Naumann M, Reiners K, Classen J (2006) Temporary occlusion of associative motor cortical plasticity by prior dynamic motor training. Cereb Cortex 16:376–385 Stinear JW, Hornby TG (2005) Stimulation-induced changes in lower limb corticomotor excitability during treadmill walking in humans. J Physiol 567:701–711 Tecchio F, Zappasodi F, Pasqualetti P, Gennaro L, Pellicciari M, Ercolani M, Squitti R, Rossini P (2008) Age dependence of primary motor cortex plasticity induced by paired associative stimulation. Clin Neurophysiol 119(3):675–682. doi:10.1016/j.clinph.2007.10.023 Ueki Y, Mima T, Kotb MA, Sawada H, Saiki H, Ikeda A, Begum T, Reza F, Nagamine T, Fukuyama H (2006) Altered plasticity of the human motor cortex in Parkinson’s disease. Ann Neurol 59:60–71 Ward NS, Swayne OB, Newton JM (2007) Age-dependent changes in the neural correlates of force modulation: an fMRI study. Neurobiol Aging (in press) Wassermann EM (2002) Variation in the response to transcranial magnetic brain stimulation in the general population. Clin Neurophysiol 113:1165–1171 Webster MJ, Herman MM, Kleinman JE, Shannon Weickert C (2006) BDNF and trkB mRNA expression in the hippocampus and temporal cortex during the human lifespan. Gene Expr Patterns 6:941–951 Weise D, Schramm A, Stefan K, Wolters A, Reiners K, Naumann M, Classen J (2006) The two sides of associative plasticity in writer’s cramp. Brain 129:2709–2721 Wolters A, Sandbrink F, Schlottmann A, Kunesch E, Stefan K, Cohen LG, Benecke R, Classen J (2003) A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol 89:2339–2345 Ziemann U, Corwell B, Cohen LG (1998) Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18:1115–1123 Ziemann U, Ilic TV, Pauli C, Meintzschel F, Ruge D (2004) Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 24:1666–1672 Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367–378