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Surround inhibition in human motor system

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Abstract

In sensory systems, a neural mechanism called surround inhibition (SI) sharpens sensation by creating an inhibitory zone around the central core of activation. In the motor system, the functional operation of SI remains to be demonstrated, although it has been hypothesized to contribute to the selection of voluntary movements. Here we test this hypothesis by using transcranial magnetic stimulation of the human motor cortex. The motor evoked potential of the little finger muscle is suppressed or unchanged during self-paced, voluntary movements of the index finger, mouth or leg, despite an increase in spinal excitability. This result indicates that motor excitability related to little finger movement is suppressed at the supraspinal level during these movements, and supports the idea that SI is an organizational principle of the motor system.

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References

  • Berardelli A (1999) Transcranial magnetic stimulation in movement disorders. Electroencephalogr Clin Neurophysiol Suppl 51:276–280

    CAS  PubMed  Google Scholar 

  • Berardelli A, Rona S, Inghilleri M, Manfredi M (1996) Cortical inhibition in Parkinson’s disease. A study with paired magnetic stimulation. Brain 119:71–77

    PubMed  Google Scholar 

  • Blakemore C, Carpenter RHS, Georgeson MA (1970) Lateral inhibition between orientation detectors in the human visual system. Nature 228:37–39

    CAS  PubMed  Google Scholar 

  • Chen R, Yaseen Z, Cohen LG, Hallett M (1998) Time course of corticospinal excitability in reaction time and self-paced movements. Ann Neurol 44:317–325

    CAS  PubMed  Google Scholar 

  • Cheney PD, Fetz EE (1985) Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimuli in primates: evidence for functional groups of CM cells. J Neurophysiol 53:786–804

    CAS  PubMed  Google Scholar 

  • Di Lazzaro V, Restuccia D, Oliviero A, Profice P, Ferrara L, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J Physiol 508:625–633

    PubMed  Google Scholar 

  • Donoghue JP, Leibovic S, Sanes JN (1992) Organization of the forelimb area in squirrel monkey motor cortex: representation of digit, wrist, and elbow muscles. Exp Brain Res 89:1–19

    CAS  PubMed  Google Scholar 

  • Filion M (2000) Physiologic basis of dyskinesia. Ann Neurol 47:S35–S40, discussion S40–41

    CAS  PubMed  Google Scholar 

  • Fisher MA (1983) F response analysis of motor disorders of central origin. J Neurol Sci 62:13–22

    Article  CAS  PubMed  Google Scholar 

  • Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257–262

    CAS  PubMed  Google Scholar 

  • Hager-Ross C, Schieber MH (2000) Quantifying the independence of human finger movements: comparisons of digits, hands, and movement frequencies. J Neurosci 20:8542–8550

    PubMed  Google Scholar 

  • Hallett M (1996) Transcranial magnetic stimulation: a useful tool for clinical neurophysiology. Ann Neurol 40:344–345

    CAS  PubMed  Google Scholar 

  • Haug BA, Kukowski B (1994) Latency and duration of the muscle silent period following transcranial magnetic stimulation in multiple sclerosis, cerebral ischemia, and other upper motoneuron lesions. Neurology 44:936–940

    CAS  PubMed  Google Scholar 

  • Hendry SH, Jones EG (1981) Sizes and distributions of intrinsic neurons incorporating tritiated GABA in monkey sensory-motor cortex. J Neurosci 1:390–408

    CAS  PubMed  Google Scholar 

  • Humphry DR (1986) Representation of movements and muscles within the primate precentral motor cortex: historical and current perspectives. Fed Proc 45:2687–2699

    CAS  PubMed  Google Scholar 

  • Huntley GW, Jones EG (1991) Relationship of intrinsic connections to forelimb movement representations in monkey motor cortex: a correlative anatomic and physiological study. J Neurophysiol 66:390–413

    CAS  PubMed  Google Scholar 

  • Kang Y, Endo K, Araki T (1991) Differential connections by intracortical axon collaterals among pyramidal tract cells in the cat motor cortex. J Physiol 435:243–256

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  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 471:501–519

    CAS  PubMed  Google Scholar 

  • Kwan HC, Murphy JT, Wong YC (1987) Interaction between neurons in precentral cortical zones controlling different joints. Brain Res 400:259–269

    Article  CAS  PubMed  Google Scholar 

  • Levy LM, Hallett M (2002) Impaired brain GABA in focal dystonia. Ann Neurol 51:93–101

    Article  CAS  PubMed  Google Scholar 

  • Liepert J, Schwenkreis P, Tegenthoff M, Malin JP (1997) The glutamate antagonist riluzole suppresses intracortical facilitation. J Neural Transm 104:1207–1214

    CAS  PubMed  Google Scholar 

  • Liepert J, Storch P, Fritsch A, Weiller C (2000) Motor cortex disinhibition in acute stroke. Clin Neurophysiol 111:671–676

    Article  CAS  PubMed  Google Scholar 

  • Maertens de Noordhout A, Pepin JL, Gerard P, Delwaide PJ (1992) Facilitation of responses to motor cortex stimulation: effects of isometric voluntary contraction. Ann Neurol 32:365–370

    PubMed  Google Scholar 

  • Matsumura M, Sawaguchi T, Oishi T, Ueki K, Kubota K (1991) Behavioral deficits induced by local injection of bicuculline and muscimol into the primate motor and premotor cortex. J Neurophysiol 65:1542–1553

    CAS  PubMed  Google Scholar 

  • Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381–425

    PubMed  Google Scholar 

  • Nagamine T, Kajola M, Salmelin R, Shibasaki H, Hari R (1996) Movement-related slow cortical magnetic fields and changes of spontaneous MEG- and EEG-brain rhythms. Electroencephalogr Clin Neurophysiol 99:274–286

    CAS  PubMed  Google Scholar 

  • Nakamura H, Kitagawa H, Kawaguchi Y, Tsuji H (1997) Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol 498:817–823

    CAS  PubMed  Google Scholar 

  • Pfleger B, Bonds AB (1995) Dynamic differentiation of GABAA-sensitive influences on orientation selectivity of complex cells in the cat striate cortex. Exp Brain Res 104:81–88

    CAS  PubMed  Google Scholar 

  • Pfurtscheller G, Lopes da Silva FH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:1842–1857

    CAS  PubMed  Google Scholar 

  • Prince DA, Wilder BJ (1967) Control mechanisms in cortical epileptogenic foci. “Surround” inhibition. Arch Neurol 16:194–202

    CAS  PubMed  Google Scholar 

  • Ridding MC, Inzelberg R, Rothwell JC (1995a) Changes in excitability of motor cortical circuitry in patients with Parkinson’s disease. Ann Neurol 37:181–188

    CAS  PubMed  Google Scholar 

  • Ridding MC, Sheean G, Rothwell JC, Inzelberg R, Kujirai T (1995b) Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. J Neurol Neurosurg Psychiatry 59:493–498

    CAS  PubMed  Google Scholar 

  • Rona S, Berardelli A, Vacca L, Inghilleri M, Manfredi M (1998) Alterations of motor cortical inhibition in patients with dystonia. Mov Disord 13:118–124

    CAS  PubMed  Google Scholar 

  • Rothwell JC (1997) Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 74:113–122

    CAS  PubMed  Google Scholar 

  • Sanes JN, Donoghue JP, Thangaraj V, Edelman RR, Warach S (1995) Shared neural substrates controlling hand movements in human motor cortex. Science 268:1775–1777

    CAS  PubMed  Google Scholar 

  • Sanger TD, Garg RR, Chen R (2001) Interactions between two different inhibitory systems in the human motor cortex. J Physiol 530:307–317

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Zarzecki P, Asanuma H (1979) Spinal branching of pyramidal tract neurons in the monkey. Exp Brain Res 34:59–72

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Yokota J, Futami T (1981) Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey. Neurosci Lett 23:7-12

    CAS  PubMed  Google Scholar 

  • Siebner HR, Dressnandt J, Auer C, Conrad B (1998) Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 21:1209–1212

    Article  CAS  PubMed  Google Scholar 

  • Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol 250:305–329

    CAS  PubMed  Google Scholar 

  • Sivilotti L, Nistri A (1991) GABA receptor mechanisms in the central nervous system. Prog Neurobiol 36:35–92

    Article  CAS  PubMed  Google Scholar 

  • Stinear CM, Byblow WD (2003) Role of intracortical inhibition in selective hand muscle activation. J Neurophysiol 89:2014–2020

    PubMed  Google Scholar 

  • Strafella AP, Valzania F, Nassetti SA, Tropeani A, Bisulli A, Santangelo M, Tassinari CA (2000) Effects of chronic levodopa and pergolide treatment on cortical excitability in patients with Parkinson’s disease: a transcranial magnetic stimulation study. Clin Neurophysiol 111:1198–1202

    Article  CAS  PubMed  Google Scholar 

  • Valls-Sole J, Pascual-Leone A, Wassermann EM, Hallett M (1992) Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol 85:355–364

    PubMed  Google Scholar 

  • Valzania F, Strafella AP, Quatrale R, Santangelo M, Tropeani A, Lucchi D, Tassinari CA, De Grandis D (1997) Motor evoked responses to paired cortical magnetic stimulation in Parkinson’s disease. Electroencephalogr Clin Neurophysiol 105:37–43

    CAS  PubMed  Google Scholar 

  • 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 (Lond) 517:591–597

    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

    CAS  PubMed  Google Scholar 

  • Ziemann U, Ishii K, Borgheresi A, Yaseen Z, Battaglia F, Hallett M, Cincotta M, Wassermann EM (1999) Dissociation of the pathways mediating ipsilateral and contralateral motor-evoked potentials in human hand and arm muscles. J Physiol 518:895–906

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Devera G. Schoenberg, MSc, for skillful editing.

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Correspondence to Mark Hallett.

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Sohn, Y.H., Hallett, M. Surround inhibition in human motor system. Exp Brain Res 158, 397–404 (2004). https://doi.org/10.1007/s00221-004-1909-y

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