Abstract
Current concepts of transcranial magnetic stimulation (TMS) over the primary motor cortex are still under debate as to whether inhibitory motor effects are exclusively of cortical origin. To further elucidate a potential subcortical influence on motor effects, we combined TMS and unilateral subcortical electrical stimulation (SES) of the corticospinal tract. SES was performed through implanted depth electrodes in eight patients treated with deep brain stimulation (DBS) for severe dystonia. Chronaxie, conduction velocity (CV) of the stimulated fibres and poststimulus time histograms of single motor unit recordings were calculated to provide evidence of an activation of large diameter myelinated fibres by SES. Excitatory and inhibitory motor effects recorded bilaterally from the first dorsal interosseus muscle were measured after SES and focal TMS of the motor cortex. This allowed us to compare motor effects of subcortical (direct) and cortical (mainly indirect) activation of corticospinal neurons. SES activated a fast conducting monosynaptic pathway to the alpha motoneuron. Motor responses elicited by SES had significantly shorter onset latency and shorter duration of the contralateral silent period compared to TMS induced motor effects. Spinal excitability as assessed by H-reflex was significantly reduced during the silent period after SES. No ipsilateral motor effects could be elicited by SES while TMS was followed by an ipsilateral inhibition. The results suggest that SES activated the corticospinal neurons at the level of the internal capsule. Comparison of SES and TMS induced motor effects reveals that the first part of the TMS induced contralateral silent period should be of spinal origin while its later part is due to cortical inhibitory mechanisms. Furthermore, the present results suggest that the ipsilateral inhibition is predominantly mediated via transcallosal pathways.
Similar content being viewed by others
References
Amassian VE, Quirk GJ, Stewart M (1990) A comparison of corticospinal activation by magnetic coil and electrical stimulation of monkey motor cortex. Electroencephalogr Clin Neurophysiol 77:390–401
Ashby P, Lang AE, Lozano AM, Dostrovsky JO (1995) Motor effects of stimulating the human cerebellar thalamus. J Physiol 489:287–298
Ashby P, Strafella A, Dostrovsky JO, Lozano A, Lang AE (1998) Immediate motor effects of stimulation through electrodes implanted in the human globus pallidus. Stereotact Funct Neurosurg 70:1–18
Ashby P, Kim YJ, Kumar R, Lang AE, Lozano AM (1999) Neurophysiological effects of stimulation through electrodes in the human subthalamic nucleus. Brain 122:1919–1931
Benabid AL, Benazzouz A, Hoffmann D, Limousin P, Krack P, Pollak P (1998) Long term electrical inhibition of deep brain targets in movement disorders. Mov Disord Suppl 3:119–125
Berardelli A, Inghilleri M, Rothwell JC, Cruccu G, Manfredi M (1991) Multiple firing of motoneurones is produced by cortical stimulation but not by direct activation of descending motor tracts. Electroencephalogr Clin Neurophysiol 81:240–242
Boroojerdi B, Diefenbach K, Ferbert A (1996) Transcallosal inhibition in cortical and subcortical cerebral vascular lesions. J Neurol Sci 144:160–170
Chen R, Lozano AM, Ashby P (1999) Mechanism of the silent period following transcranial magnetic stimulation. Evidence from epidural recordings. Exp Brain Res 128:539–542
Classen J, Benecke R (1995) Inhibitory phenomena in individual motor units induced by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 97:264–274
Desmedt JE, Cheron G (1983) Spinal and far-field components of human somatosensory evoked potentials to posterior tibial nerve stimulation analysed with oesophageal derivations and non-cephalic reference recording. Electroencephalogr Clin Neurophysiol 56:635–651
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 124:520–524
Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD (1992) Interhemispheric inhibition of the human motor cortex. J Physiol 453:525–546
Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257–262
Gerloff C, Cohen LG, Floeter MK, Chen R, Corwell B, Hallett M (1998) Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract. J Physiol 510:249–259
Giesen HJ von, Roick H, Benecke R (1994) Inhibitory actions of motor cortex following unilateral brain lesions as studied by magnetic brain stimulation. Exp Brain Res 99:84–96
Holsheimer J, Dijkstra EA, Demeulemeester H, Nuttin B (2000) Chronaxie calculated from current-duration and voltage-duration data. J Neurosci Methods 97:45–50
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
Kühn AA, Kupsch A, Trottenberg T, Meyer B (2002) Pseudo-bilateral hand motor responses evoked by magnetic cortex stimulation in patients with implanted GPI-electrodes. Clin Neurophysiol 113:341–345
Kühn AA, Meyer BU, Trottenberg T, Brandt SA, Schneider GH, Kupsch A (2003) Modulation of motor cortex excitability by pallidal stimulation in patients with severe dystonia. Neurology 60:768–774
Kumar R, Chen R, Ashby P (1999) Safety of transcranial magnetic stimulation in patients with implanted deep brain stimulators. Mov Disord 14:157–158
Meyer BU, Roricht S, Grafin von Einsiedel, Kruggel F, Weindl A (1995) Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain 118:429–440
Priori A, Berardelli A, Mercuri B, Inghilleri M, Manfredi M (1995) The effect of hyperventilation on motor cortical inhibition in humans: a study of the electromyographic silent period evoked by transcranial brain stimulation. Electroencephalogr Clin Neurophysiol 97:69–72
Ranck JBJ (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417–440
Roick H, von Giesen HJ, Benecke R (1993) On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects. Exp Brain Res 94:489–498
Röricht S, Irlbacher K, Petrow E, Meyer B-U (1997) Normwerte transkallosal und kortikospinal vermittelter EMG-Effekte einer hemisphärenselektiven magnetischen Kortexreizung beim Menschen. Z EEG-EMG 28:34–38
Rothwell J, Burke D, Hicks R, Stephen J, Woodforth I, Crawford M (1994) Transcranial electrical stimulation of the motor cortex in man: further evidence for the site of activation. J Physiol 481:243–250
Sanger TD, Garg RR, Chen R (2001) Interactions between two different inhibitory systems in the human motor cortex. J Physiol 530:307–317
Schnitzler A, Benecke R (1994) The silent period after transcranial magnetic stimulation is of exclusive cortical origin: evidence from isolated cortical ischemic lesions in man. Neurosci Lett 180:41–45
Schnitzler A, Kessler KR, Benecke R (1996) Transcallosally mediated inhibition of interneurons within human primary motor cortex. Exp Brain Res 112:381–391
Stoney SDJ, Thompson WD, Asanuma H (1968) Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. J Neurophysiol 31:659–669
Ugawa Y (1999) Stimulation at the foramen magnum level. Electroencephalogr Clin Neurophysiol Suppl 51:65–75
Ugawa Y, Rothwell JC, Day BL, Thompson PD, Marsden CD (1991) Percutaneous electrical stimulation of corticospinal pathways at the level of the pyramidal decussation in humans. Ann Neurol 29:418–427
Uncini A, Treviso M, Di Muzio A, Simone P, Pullman S (1993) Physiological basis of voluntary activity inhibition induced by transcranial cortical stimulation. Electroencephalogr Clin Neurophysiol 89:211–220
Wassermann EM, Fuhr P, Cohen LG, Hallett M (1991) Effects of transcranial magnetic stimulation on ipsilateral muscles. Neurology 41:1795–1799
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 517:591–597
Ziemann U, Hallett M (2000) Basic neurophysiological studies with TMS. In: George MS, Belmarker RH (eds) Transcranial magnetic stimulation in neuropsychiatry. American Psychiatric Press, Washington DC, pp 45–98
Ziemann U, Netz J, Szelenyi A, Homberg V (1993) Spinal and supraspinal mechanisms contribute to the silent period in the contracting soleus muscle after transcranial magnetic stimulation of human motor cortex. Neurosci Lett 156:167–171
Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996) The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 109:127–135
Acknowledgement
We gratefully acknowledge critical comments on the manuscript by Dr. Peter Brown.
Author information
Authors and Affiliations
Corresponding author
Additional information
This paper is dedicated to Bernd-Ulrich Meyer, who died in a plane accident
Rights and permissions
About this article
Cite this article
Kühn, A.A., Brandt, S.A., Kupsch, A. et al. Comparison of motor effects following subcortical electrical stimulation through electrodes in the globus pallidus internus and cortical transcranial magnetic stimulation. Exp Brain Res 155, 48–55 (2004). https://doi.org/10.1007/s00221-003-1707-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-003-1707-y