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Hemispheric asymmetry and somatotopy of afferent inhibition in healthy humans

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Abstract

A conditioning electrical stimulus to a digital nerve can inhibit the motor-evoked potentials (MEPs) in adjacent hand muscles elicited by transcranial magnetic stimulation (TMS) to the contralateral primary motor cortex (M1) when given 25–50 ms before the TMS pulse. This is referred to as short-latency afferent inhibition (SAI). We studied inter-hemispheric differences (Experiment 1) and within-limb somatotopy (Experiment 2) of SAI in healthy right-handers. In Experiment 1, conditioning electrical pulses were applied to the right or left index finger (D2) and MEPs were recorded from relaxed first dorsal interosseus (FDI) and abductor digiti minimi (ADM) muscles ipsilateral to the conditioning stimulus. We found that SAI was more pronounced in right hand muscles. In Experiment 2, electrical stimulation was applied to the right D2 and MEPs were recorded from ipsilateral FDI, extensor digitorum communis (EDC) and biceps brachii (BB) muscles. The amount of SAI did not differ between FDI, EDC and BB muscles. These data demonstrate inter-hemispheric differences in the processing of cutaneous input from the hand, with stronger SAI in the dominant left hemisphere. We also found that SAI occurred not only in hand muscles adjacent to electrical digital stimulation, but also in distant hand and forearm and also proximal arm muscles. This suggests that SAI induced by electrical D2 stimulation is not focal and somatotopically specific, but a more widespread inhibitory phenomenon.

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References

  • Amunts K, Schlaug G, Schleicher A, Steinmetz H, Dabringhaus A, Roland PE, Zilles K (1996) Asymmetry in the human motor cortex and handedness. Neuroimage 4:216–222

    Article  PubMed  CAS  Google Scholar 

  • Asanuma H, Pavlides C (1997) Neurobiological basis of motor learning in mammals. Neuroreport 8:i–vi

    PubMed  CAS  Google Scholar 

  • Beisteiner R, Windischberger C, Lanzenberger R, Edward V, Cunnington R, Erdler M, Gartus A, Streibl B, Moser E, Deecke L (2001) Finger somatotopy in human motor cortex. Neuroimage 13:1016–1026

    Article  PubMed  CAS  Google Scholar 

  • Buchel C, Raedler T, Sommer M, Sach M, Weiller C, Koch MA (2004) White matter asymmetry in the human brain: a diffusion tensor MRI study. Cereb Cortex 14:945–951

    Article  PubMed  CAS  Google Scholar 

  • Buchner H, Ludwig I, Waberski T, Wilmes K, Ferbert A (1995) Hemispheric asymmetries of early cortical somatosensory evoked potentials revealed by topographic analysis. Electromyogr Clin Neurophysiol 35:207–215

    PubMed  CAS  Google Scholar 

  • Civardi C, Cavalli A, Naldi P, Varrasi C, Cantello R (2000) Hemispheric asymmetries of cortico-cortical connections in human hand motor areas. Clin Nurophysiol 111:624–629

    Article  CAS  Google Scholar 

  • Classen J, Steinfelder B, Liepert J, Stefan K, Celnik P, Cohen LG, Hess A, Kunesch E, Chen R, Benecke R, Hallett M (2000) Cutaneomotor integration in humans is somatotopically organized at various levels of the nervous system and is task dependent. Exp Brain Res 130:48–59

    Article  PubMed  CAS  Google Scholar 

  • Dassonville P, Zhu XH, Uurbil K, Kim SG, Ashe J (1997) Functional activation in motor cortex reflects the direction and the degree of handedness. Proc Natl Acad Sci USA 94:14015–14018

    Article  PubMed  CAS  Google Scholar 

  • Day BL, Riescher H, Struppler A, Rothwell JC, Marsden CD (1991) Changes in the response to magnetic and electrical stimulation of the motor cortex following muscle stretch in man. J Physiol (Lond) 433:41–57

    CAS  Google Scholar 

  • Dechent P, Frahm J (2003) Functional somatotopy of finger representations in human primary motor cortex. Hum Brain Mapp 18:272–283

    Article  PubMed  Google Scholar 

  • Delwaide PJ, Olivier E (1990) Conditioning transcranial cortical stimulation (TCCS) by exteroceptive stimulation in parkinsonian patients. Adv Neurol 53:175–181

    PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Di Giovanni S, Zito G, Tonali P, Rothwell JC (2000) Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Exp Brain Res 135:455–461

    Article  PubMed  CAS  Google Scholar 

  • Floeter MK, Gerloff C, Kouri J, Hallett M (1998) Cutaneous withdrawal reflexes of the upper extremity. Muscle Nerve 21:591–598

    Article  PubMed  CAS  Google Scholar 

  • Graziano MS, Taylor CS, Moore T, Cooke DF (2002) The cortical control of movement revisited. Neuron 36:349–362

    Article  PubMed  CAS  Google Scholar 

  • Hammond G, Faulkner D, Byrnes M, Mastaglia F, Thickbroom G (2004) Transcranial magnetic stimulation reveals asymmetrical efficacy of intracortical circuits in primary motor cortex. Exp Brain Res 155:19–23

    Article  PubMed  Google Scholar 

  • Ilic TV, Meintzschel F, Cleff U, Ruge D, Kessler KR, Ziemann U (2002) Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol 545:153–167

    Article  PubMed  CAS  Google Scholar 

  • Ilic TV, Jung P, Ziemann U (2004) Subtle hemispheric asymmetry of motor cortical inhibitory tone. Clin Neurophysiol 115:330–340

    Article  PubMed  Google Scholar 

  • Keller A (1993) Intrinsic synaptic organization of the motor cortex. Cereb Cortex 3:430–441

    Article  PubMed  CAS  Google Scholar 

  • Krause T, Kurth R, Ruben J, Schwiemann J, Villringer K, Deuchert M, Moosmann M, Brandt S, Wolf K, Curio G, Villringer A (2001) Representational overlap of adjacent fingers in multiple areas of human primary somatosensory cortex depends on electrical stimulus intensity: an fMRI study. Brain Res 899:36–46

    Article  PubMed  CAS  Google Scholar 

  • Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol (Lond) 471:501–519

    CAS  Google Scholar 

  • Kurth R, Villringer K, Curio G, Wolf KJ, Krause T, Repenthin J, Schwiemann J, Deuchert M, Villringer A (2000) fMRI shows multiple somatotopic digit representations in human primary somatosensory cortex. Neuroreport 11:1487–1491

    Article  PubMed  CAS  Google Scholar 

  • Maertens de Noordhout A, Rothwell JC, Day BL, Dressler D, Nakashima K, Thompson PD, Marsden CD (1992) Effect of digital nerve stimuli on responses to electrical or magnetic stimulation of the human brain. J Physiol (Lond) 447:535–548

    CAS  Google Scholar 

  • Manganotti P, Zanette G, Bonato C, Tinazzi M, Polo A, Fiaschi A (1997) Crossed and direct effects of digital nerves stimulation on motor evoked potential: a study with magnetic brain stimulation. Electroencephalogr Clin Neurophysiol 105:280–289

    Article  PubMed  CAS  Google Scholar 

  • Netz J, Ziemann U, Homberg V (1995) Hemispheric asymmetry of transcallosal inhibition in man. Exp Brain Res 104:527–533

    Article  PubMed  CAS  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Palmer E, Ashby P (1992) The transcortical nature of the late reflex responses in human small hand muscle to digital nerve stimulation. Exp Brain Res 91:320–326

    Article  PubMed  CAS  Google Scholar 

  • Pujol J, Lopez-Sala A, Deus J, Cardoner N, Sebastian-Galles N, Conesa G, Capdevila A (2002) The lateral asymmetry of the human brain studied by volumetric magnetic resonance imaging. Neuroimage 17:670–679

    Article  PubMed  Google Scholar 

  • Reis J, Tergau F, Hamer HM, Muller HH, Knake S, Fritsch B, Oertel WH, Rosenow F (2002) Topiramate selectively decreases intracortical excitability in human motor cortex. Epilepsia 43:1149–1156

    Article  PubMed  CAS  Google Scholar 

  • Ridding MC, Pearce SL, Flavel SC (2005) Modulation of intracortical excitability in human hand motor areas. The effect of cutaneous stimulation and its topographical arrangement. Exp Brain Res 163:335–343

    Article  PubMed  CAS  Google Scholar 

  • Rizzolatti G, Luppino G, Matelli M (1998) The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol. 106:283–296

    Article  PubMed  CAS  Google Scholar 

  • Ruben J, Schwiemann J, Deuchert M, Meyer R, Krause T, Curio G, Villringer K, Kurth R, Villringer A (2001) Somatotopic organization of human secondary somatosensory cortex. Cereb Cortex 11:463–473

    Article  PubMed  CAS  Google Scholar 

  • Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R (2003) Short and long latency afferent inhibition in Parkinson’s disease. Brain 126:1883–1894

    Article  PubMed  Google Scholar 

  • Schieber MH (2001) Constraints on somatotopic organization in the primary motor cortex. J Neurophysiol 86:2125–2143

    PubMed  CAS  Google Scholar 

  • Tamburin S, Manganotti P, Zanette G, Fiaschi A (2001) Cutaneomotor integration in human hand motor areas: somatotopic effect and interaction of afferents. Exp Brain Res 141:232–241

    Article  PubMed  CAS  Google Scholar 

  • Tamburin S, Manganotti P, Marzi CA, Fiaschi A, Zanette G (2002) Abnormal somatotopic arrangement of sensorimotor interactions in dystonic patients. Brain 125:2719–2730

    Article  PubMed  Google Scholar 

  • Tamburin S, Fiaschi A, Andreoli A, Forgione A, Manganotti P, Zanette G (2003a) Abnormal cutaneomotor integration in patients with cerebellar syndromes: a transcranial magnetic stimulation study. Clin Neurophysiol 114:643–651

    Article  PubMed  Google Scholar 

  • Tamburin S, Fiaschi A, Idone D, Lochner P, Manganotti P, Zanette G (2003b) Abnormal sensorimotor integration is related to disease severity in Parkinson’s disease: a TMS study. Mov Disord 18:1316–1324

    Article  PubMed  Google Scholar 

  • Tokimura H, Di Lazzaro V, Tokimura Y, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (2000) Short latency inhibition of human hand motor cortex by somatosensory input from the hand [published erratum appears in J Physiol (Lond) 2000 523:503–513

    Google Scholar 

  • Triggs WJ, Subramanium B, Rossi F (1999) Hand preference and transcranial magnetic stimulation asymmetry of cortical motor representation. Brain Res 835:324–329

    Article  PubMed  CAS  Google Scholar 

  • Volkmann J, Schnitzler A, Witte OW, Freund H (1998) Handedness and asymmetry of hand representation in human motor cortex. J Neurophysiol 79:2149–2154

    PubMed  CAS  Google Scholar 

  • van Westen D, Fransson P, Olsrud J, Rosen B, Lundborg G, Larsson EM (2004) Fingersomatotopy in area 3b: an fMRI-study. BMC Neurosci 5:28

    Article  PubMed  Google Scholar 

  • Yahagi S, Kasai T (1999) Motor evoked potentials induced by motor imagery reveal a functional asymmetry of cortical motor control in. Neurosci Lett 276:185–188

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

RCG Helmich was sponsored by De Nederlandse Vereniging voor Dystonie Patiënten, De Hersenstichting Nederland, De Fundatie van de Vrijvrouwe van Renswoude and Stichting Nijmeegs Universiteits Fonds (SNUF). A. Münchau and H.R. Siebner were supported by the Volkswagenstiftung and A. Münchau also by the Forschungsförderungs-Fond of the Hamburg University Hospital. We wish to thank the reviewers of this paper for their thoughtful and constructive criticism. Experiment 2 was redesigned on the basis of their suggestions. We also thank Melanie Jonas for statistical advice.

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Authors and Affiliations

  1. Department of Neurology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands

    R. C. G. Helmich & B. R. Bloem

  2. Department of Neurology, Hamburg University Hospital, Martinistrasse 52, 20246, Hamburg, Germany

    T. Bäumer & A. Münchau

  3. Department of Neurology, Christian-Albrechts-University, Kiel, Germany

    H. R. Siebner

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  1. R. C. G. Helmich
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  2. T. Bäumer
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  3. H. R. Siebner
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  4. B. R. Bloem
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  5. A. Münchau
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Correspondence to T. Bäumer.

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R.C.G. Helmich, T. Bäumer both authors contributed equally to this work

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Helmich, R.C.G., Bäumer, T., Siebner, H.R. et al. Hemispheric asymmetry and somatotopy of afferent inhibition in healthy humans. Exp Brain Res 167, 211–219 (2005). https://doi.org/10.1007/s00221-005-0014-1

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