Skip to main content
Top
Published in: Experimental Brain Research 1/2008

Open Access 01-03-2008 | Research Article

The effect of age on task-related modulation of interhemispheric balance

Authors: P. Talelli, W. Waddingham, A. Ewas, J. C. Rothwell, N. S. Ward

Published in: Experimental Brain Research | Issue 1/2008

Login to get access

Abstract

Normal aging is associated with less lateralised task-related activation of the primary motor cortices. It has been hypothesized, but not tested, that this phenomenon is mediated transcallosaly. We have used Transcranial Magnetic Stimulation to look for age-related changes in interhemispheric inhibition (IHI). Thirty healthy individuals (aged 19–78 years) were studied using a paired-pulse protocol at rest and during a low-strength isometric contraction with the right hand. The IHI targeting the right motor cortex was assessed at two intervals, 10 ms (IHI10) and 40 ms (IHI40). The corticospinal excitability of the left hemisphere was assessed by means of input–output curves constructed during voluntary construction. Age was not correlated with IHI10 or IHI40 at rest. During muscle contraction IHI tended to increase at both intervals. However, this increase in IHI during the active condition (changeIHI) was less evident with advancing age for the 40 ms interval (r = 0.444, P = 0.02); in fact a degree of disinhibition was often present. There was no correlation between age and changeIHI10. Age was negatively correlated with the area under the recruitment curve (r = −0.585, P = 0.001) and the size of the maximum MEP collected (r = −0.485, P = 0.007). ChangeIHI and measures of corticospinal excitability were not intercorrelated. In conclusion, task-related increases in interhemispheric inhibition seem to diminish with advancing age. This phenomenon is specific for long-latency IHI and may underlie the age-related bihemispheric activation seen in functional imaging studies. The mechanism underlying changes in IHI with advancing age and the association with changes in corticospinal excitability need further investigation.
Literature
go back to reference Capaday C, Lavoie BA, Barbeau H, Schneider C, Bonnard M (1999) Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. J Neurophysiol 81:129–139PubMed Capaday C, Lavoie BA, Barbeau H, Schneider C, Bonnard M (1999) Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. J Neurophysiol 81:129–139PubMed
go back to reference Chen R (2004) Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res 154:1–10PubMedCrossRef Chen R (2004) Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res 154:1–10PubMedCrossRef
go back to reference Chen R, Yung D, Li JY (2003) Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. J Neurophysiol 89:1256–1264PubMedCrossRef Chen R, Yung D, Li JY (2003) Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. J Neurophysiol 89:1256–1264PubMedCrossRef
go back to reference Daskalakis ZJ, Christensen BK, Fitzgerald PB, Roshan L, Chen R (2002) The mechanisms of interhemispheric inhibition in the human motor cortex. J Physiol 543:317–326PubMedCrossRef Daskalakis ZJ, Christensen BK, Fitzgerald PB, Roshan L, Chen R (2002) The mechanisms of interhemispheric inhibition in the human motor cortex. J Physiol 543:317–326PubMedCrossRef
go back to reference Day BL, Dressler D, Maertens dN, Marsden CD, Nakashima K, Rothwell JC, Thompson PD (1989) Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. J Physiol 412:449–473PubMed Day BL, Dressler D, Maertens dN, Marsden CD, Nakashima K, Rothwell JC, Thompson PD (1989) Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. J Physiol 412:449–473PubMed
go back to reference De Gennaro L, Bertini M, Pauri F, Cristiani R, Curcio G, Ferrara M, Rossini PM (2004) Callosal effects of transcranial magnetic stimulation (TMS): the influence of gender and stimulus parameters. Neurosci Res 48:129–137PubMedCrossRef De Gennaro L, Bertini M, Pauri F, Cristiani R, Curcio G, Ferrara M, Rossini PM (2004) Callosal effects of transcranial magnetic stimulation (TMS): the influence of gender and stimulus parameters. Neurosci Res 48:129–137PubMedCrossRef
go back to reference Delbono O, O’Rourke KS, Ettinger WH (1995) Excitation-calcium release uncoupling in aged single human skeletal muscle fibers. J Membr Biol 148:211–222PubMed Delbono O, O’Rourke KS, Ettinger WH (1995) Excitation-calcium release uncoupling in aged single human skeletal muscle fibers. J Membr Biol 148:211–222PubMed
go back to reference Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338PubMedCrossRef Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338PubMedCrossRef
go back to reference Di Lazzaro V, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (1999) Direct demonstration of interhemispheric inhibition of the human motor cortex produced by transcranial magnetic stimulation. Exp Brain Res 124:520–524PubMedCrossRef Di Lazzaro V, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (1999) Direct demonstration of interhemispheric inhibition of the human motor cortex produced by transcranial magnetic stimulation. Exp Brain Res 124:520–524PubMedCrossRef
go back to reference Dorfman LJ, Bosley TM (1979) Age-related changes in peripheral and central nerve conduction in man. Neurology 29:38–44PubMed Dorfman LJ, Bosley TM (1979) Age-related changes in peripheral and central nerve conduction in man. Neurology 29:38–44PubMed
go back to reference Duque J, Mazzocchio R, Dambrosia J, Murase N, Olivier E, Cohen LG (2005) Kinematically specific interhemispheric inhibition operating in the process of generation of a voluntary movement. Cereb Cortex 15:588–593PubMedCrossRef Duque J, Mazzocchio R, Dambrosia J, Murase N, Olivier E, Cohen LG (2005) Kinematically specific interhemispheric inhibition operating in the process of generation of a voluntary movement. Cereb Cortex 15:588–593PubMedCrossRef
go back to reference Duque J, Murase N, Celnik P, Hummel F, Harris-Love M, Mazzocchio R, Olivier E, Cohen LG (2007) Intermanual Differences in movement-related interhemispheric inhibition. J Cogn Neurosci 19:204–213PubMedCrossRef Duque J, Murase N, Celnik P, Hummel F, Harris-Love M, Mazzocchio R, Olivier E, Cohen LG (2007) Intermanual Differences in movement-related interhemispheric inhibition. J Cogn Neurosci 19:204–213PubMedCrossRef
go back to reference Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD (1992) Interhemispheric inhibition of the human motor cortex. J Physiol 453:525–546PubMed Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD (1992) Interhemispheric inhibition of the human motor cortex. J Physiol 453:525–546PubMed
go back to reference Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG (1998) The role of the human motor cortex in the control of complex and simple finger movement sequences. Brain 121:1695–1709PubMedCrossRef Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG (1998) The role of the human motor cortex in the control of complex and simple finger movement sequences. Brain 121:1695–1709PubMedCrossRef
go back to reference Hackel ME, Wolfe GA, Bang SM, Canfield JS (1992) Changes in hand function in the aging adult as determined by the Jebsen test of hand function. Phys Ther 72:373–377PubMed Hackel ME, Wolfe GA, Bang SM, Canfield JS (1992) Changes in hand function in the aging adult as determined by the Jebsen test of hand function. Phys Ther 72:373–377PubMed
go back to reference Haug H, Eggers R (1991) Morphometry of the human cortex cerebri and corpus striatum during aging. Neurobiol Aging 12:336–338PubMedCrossRef Haug H, Eggers R (1991) Morphometry of the human cortex cerebri and corpus striatum during aging. Neurobiol Aging 12:336–338PubMedCrossRef
go back to reference Hortobagyi T, Devita P (2006) Mechanisms responsible for the age-associated increase in coactivation of antagonist muscles. Exerc Sport Sci Rev 34:29–35PubMedCrossRef Hortobagyi T, Devita P (2006) Mechanisms responsible for the age-associated increase in coactivation of antagonist muscles. Exerc Sport Sci Rev 34:29–35PubMedCrossRef
go back to reference Hortobagyi T, del Olmo MF, Rothwell JC (2006) Age reduces cortical reciprocal inhibition in humans. Exp Brain Res 171:322–329PubMedCrossRef Hortobagyi T, del Olmo MF, Rothwell JC (2006) Age reduces cortical reciprocal inhibition in humans. Exp Brain Res 171:322–329PubMedCrossRef
go back to reference Hutchinson S, Kobayashi M, Horkan CM, Pascual-Leone A, Alexander MP, Schlaug G (2002) Age-related differences in movement representation. Neuroimage 17:1720–1728PubMedCrossRef Hutchinson S, Kobayashi M, Horkan CM, Pascual-Leone A, Alexander MP, Schlaug G (2002) Age-related differences in movement representation. Neuroimage 17:1720–1728PubMedCrossRef
go back to reference Irlbacher K, Brocke J, Mechow JV, Brandt SA (2007) Effects of GABA(A) and GABA(B) agonists on interhemispheric inhibition in man. Clin Neurophysiol 118:308–316PubMedCrossRef Irlbacher K, Brocke J, Mechow JV, Brandt SA (2007) Effects of GABA(A) and GABA(B) agonists on interhemispheric inhibition in man. Clin Neurophysiol 118:308–316PubMedCrossRef
go back to reference Kido A, Tanaka N, Stein RB (2004) Spinal excitation and inhibition decrease as humans age. Can J Physiol Pharmacol 82:238–248PubMedCrossRef Kido A, Tanaka N, Stein RB (2004) Spinal excitation and inhibition decrease as humans age. Can J Physiol Pharmacol 82:238–248PubMedCrossRef
go back to reference Kossev AR, Schrader C, Dauper J, Dengler R, Rollnik JD (2002) Increased intracortical inhibition in middle-aged humans; a study using paired-pulse transcranial magnetic stimulation. Neurosci Lett 333:83–86PubMedCrossRef Kossev AR, Schrader C, Dauper J, Dengler R, Rollnik JD (2002) Increased intracortical inhibition in middle-aged humans; a study using paired-pulse transcranial magnetic stimulation. Neurosci Lett 333:83–86PubMedCrossRef
go back to reference Kukaswadia S, Wagle-Shukla A, Morgante F, Gunraj C, Chen R (2005) Interactions between long latency afferent inhibition and interhemispheric inhibitions in the human motor cortex. J Physiol 563:915–924PubMedCrossRef Kukaswadia S, Wagle-Shukla A, Morgante F, Gunraj C, Chen R (2005) Interactions between long latency afferent inhibition and interhemispheric inhibitions in the human motor cortex. J Physiol 563:915–924PubMedCrossRef
go back to reference Lee H, Gunraj C, Chen R (2007) The effects of inhibitory and facilitatory intracortical circuits on interhemispheric inhibition in the human motor cortex. J Physiol 580:1021–1032PubMedCrossRef Lee H, Gunraj C, Chen R (2007) The effects of inhibitory and facilitatory intracortical circuits on interhemispheric inhibition in the human motor cortex. J Physiol 580:1021–1032PubMedCrossRef
go back to reference Leocani L, Cohen LG, Wassermann EM, Ikoma K, Hallett M (2000) Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. Brain 123(Pt 6):1161–1173PubMedCrossRef Leocani L, Cohen LG, Wassermann EM, Ikoma K, Hallett M (2000) Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. Brain 123(Pt 6):1161–1173PubMedCrossRef
go back to reference Liepert J, Dettmers C, Terborg C, Weiller C (2001) Inhibition of ipsilateral motor cortex during phasic generation of low force. Clin Neurophysiol 112:114–121PubMedCrossRef Liepert J, Dettmers C, Terborg C, Weiller C (2001) Inhibition of ipsilateral motor cortex during phasic generation of low force. Clin Neurophysiol 112:114–121PubMedCrossRef
go back to reference Madden DJ, Whiting WL, Huettel SA, White LE, MacFall JR, Provenzale JM (2004) Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time. Neuroimage 21:1174–1181PubMedCrossRef Madden DJ, Whiting WL, Huettel SA, White LE, MacFall JR, Provenzale JM (2004) Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time. Neuroimage 21:1174–1181PubMedCrossRef
go back to reference Minati L, Grisoli M, Bruzzone MG (2007) MR spectroscopy, functional MRI, and diffusion-tensor imaging in the aging brain: a conceptual review. J Geriatr Psychiatry Neurol 20:3–21PubMedCrossRef Minati L, Grisoli M, Bruzzone MG (2007) MR spectroscopy, functional MRI, and diffusion-tensor imaging in the aging brain: a conceptual review. J Geriatr Psychiatry Neurol 20:3–21PubMedCrossRef
go back to reference Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409PubMedCrossRef Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409PubMedCrossRef
go back to reference Naccarato M, Calautti C, Jones PS, Day DJ, Carpenter TA, Baron JC (2006) Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study. Neuroimage 32:1250–1256PubMedCrossRef Naccarato M, Calautti C, Jones PS, Day DJ, Carpenter TA, Baron JC (2006) Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study. Neuroimage 32:1250–1256PubMedCrossRef
go back to reference 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 55:74–77PubMedCrossRef 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 55:74–77PubMedCrossRef
go back to reference 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 313:33–36PubMedCrossRef 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 313:33–36PubMedCrossRef
go back to reference Pitcher JB, Ogston KM, Miles TS (2003) Age and sex differences in human motor cortex input-output characteristics. J Physiol 546:605–613PubMedCrossRef Pitcher JB, Ogston KM, Miles TS (2003) Age and sex differences in human motor cortex input-output characteristics. J Physiol 546:605–613PubMedCrossRef
go back to reference Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1986) Numerical recipes. Cambridge University Press, Cambridge Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1986) Numerical recipes. Cambridge University Press, Cambridge
go back to reference Sale MV, Semmler JG (2005) Age-related differences in corticospinal control during functional isometric contractions in left and right hands. J Appl Physiol 99:1483–1493PubMedCrossRef Sale MV, Semmler JG (2005) Age-related differences in corticospinal control during functional isometric contractions in left and right hands. J Appl Physiol 99:1483–1493PubMedCrossRef
go back to reference Smith CD, Umberger GH, Manning EL, Slevin JT, Wekstein DR, Schmitt FA, Markesbery WR, Zhang Z, Gerhardt GA, Kryscio RJ, Gash DM (1999) Critical decline in fine motor hand movements in human aging. Neurology 53:1458–1461PubMed Smith CD, Umberger GH, Manning EL, Slevin JT, Wekstein DR, Schmitt FA, Markesbery WR, Zhang Z, Gerhardt GA, Kryscio RJ, Gash DM (1999) Critical decline in fine motor hand movements in human aging. Neurology 53:1458–1461PubMed
go back to reference Talelli P, Greenwood RJ, Rothwell JC (2006) Arm function after stroke: neurophysiological correlates and recovery mechanisms assessed by transcranial magnetic stimulation. Clin Neurophysiol 117:1641–1659PubMedCrossRef Talelli P, Greenwood RJ, Rothwell JC (2006) Arm function after stroke: neurophysiological correlates and recovery mechanisms assessed by transcranial magnetic stimulation. Clin Neurophysiol 117:1641–1659PubMedCrossRef
go back to reference Wang FC, de Pasqua V, Delwaide PJ (1999) Age-related changes in fastest and slowest conducting axons of thenar motor units. Muscle Nerve 22:1022–1029PubMedCrossRef Wang FC, de Pasqua V, Delwaide PJ (1999) Age-related changes in fastest and slowest conducting axons of thenar motor units. Muscle Nerve 22:1022–1029PubMedCrossRef
go back to reference Ward NS, Frackowiak RS (2003) Age-related changes in the neural correlates of motor performance. Brain 126:873–888PubMedCrossRef Ward NS, Frackowiak RS (2003) Age-related changes in the neural correlates of motor performance. Brain 126:873–888PubMedCrossRef
go back to reference Ward NS, Cohen LG (2004) Mechanisms underlying recovery of motor function after stroke. Arch Neurol 61:1844–1848PubMedCrossRef Ward NS, Cohen LG (2004) Mechanisms underlying recovery of motor function after stroke. Arch Neurol 61:1844–1848PubMedCrossRef
go back to reference Ward NS, Swayne OB, Newton JM (2007) Age-dependent changes in the neural correlates of force modulation: An fMRI study. Neurobiol Aging June 11 Ward NS, Swayne OB, Newton JM (2007) Age-dependent changes in the neural correlates of force modulation: An fMRI study. Neurobiol Aging June 11
go back to reference Wassermann EM (2002) Variation in the response to transcranial magnetic brain stimulation in the general population. Clin Neurophysiol 113:1165–1171PubMedCrossRef Wassermann EM (2002) Variation in the response to transcranial magnetic brain stimulation in the general population. Clin Neurophysiol 113:1165–1171PubMedCrossRef
Metadata
Title
The effect of age on task-related modulation of interhemispheric balance
Authors
P. Talelli
W. Waddingham
A. Ewas
J. C. Rothwell
N. S. Ward
Publication date
01-03-2008
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 1/2008
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-007-1205-8

Other articles of this Issue 1/2008

Experimental Brain Research 1/2008 Go to the issue