Experimental Brain Research

, Volume 154, Issue 2, pp 218–225 | Cite as

Changes in corticospinal motor excitability induced by non-motor linguistic tasks

  • I. Papathanasiou
  • S. R. Filipović
  • R. Whurr
  • J. C. Rothwell
  • M. Jahanshahi
Research Article

Abstract

The excitability of the corticospinal motor pathways to transcranial magnetic stimulation (TMS) can be differentially modulated by a variety of motor tasks. However, there is emerging evidence that linguistic tasks may alter excitability of the corticospinal motor pathways also. In this study we evaluated the effect of several movement-free, low-level linguistic processes involved in reading and writing on the excitability of the bilateral corticospinal motor pathways in a group of right-handed subjects. The study included two series of tasks, visual searching/matching and imaginal writing/drawing. The tasks were designed to roughly correspond with elemental aspects of the reading and writing, grapheme recognition and grapheme generation, respectively. Each task series included separate blocks with different task targets: letters, digits, semantically easy-to-code (i.e. geometric) shapes, and semantically hard-to-code shapes, as well as control blocks with no task. During task performance, TMS was delivered randomly over the hand area of either the left or right motor cortex and the modulation of the excitability of the corticospinal motor pathways was measured bilaterally through changes of the size of the motor-evoked potential (MEP) induced in the relaxed right and left first dorsal interosseous (FDI) muscles. We found that the size of the MEP in hand muscles increased during visual searching/matching tasks, particularly when targets were letters or geometric shapes, and the increase was significant for the dominant hand (left hemisphere) only. No such consistent effects were seen across subjects during imaginal tasks. This study provides evidence that even the performance of certain low-level linguistic tasks can modulate the excitability of the corticospinal motor pathways, particularly those originating from the left (dominant) hemisphere, despite the absence of overt motor activity. Moreover, in the light of the recently increased awareness of the role of “mirror neurons” in perception, the results suggest that activation of motor circuits used in generation of the written output may be an essential part of the perception of the written material as well. Understanding the patterns of task-dependent changes in excitability of the corticospinal motor pathways will provide insights into the organisation of central nervous system functional networks involved in linguistic processes, and may also be useful for future development of novel approaches to rehabilitation therapy of linguistic and motor functions.

Keywords

Linguistic functions Transcranial magnetic stimulation Cortical excitability Laterality 

References

  1. Baldissera F, Cavallari P, Craighero L, Fadiga L (2001) Modulation of spinal excitability during observation of hand actions in humans. Eur J Neurosci 13:190–194CrossRefPubMedGoogle Scholar
  2. Beauregard M, Chertkow H, Bub D et al. (1997) The neural substrate for concrete, abstract, and emotional word lexica: a positron emission tomography study. J Cogn Neurosci 9:441–461Google Scholar
  3. Brown H, Kosslyn S (1993) Cerebral lateralization. Curr Opin Neurobiol 3:183–186Google Scholar
  4. Dean P (1976) Effects of inferotemporal lesions on the behaviour of monkeys. Psychol Bull 83:41–71CrossRefPubMedGoogle Scholar
  5. Decety J, Grezes J, Costes N, Perani D, Jeannerod M, Procyk E, Grassi F, Fazio F (1997) Brain activity during observation of actions. Influence of action content and subject’s strategy. Brain 120: 1763–1777PubMedGoogle Scholar
  6. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73:2608–2611PubMedGoogle Scholar
  7. Fadiga L, Buccino G, Craighero L, Fogassi L, Gallese V, Pavesi G (1999) Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study. Neuropsychologia 37:147–158CrossRefPubMedGoogle Scholar
  8. Fadiga L, Craighero L, Buccino G, Rizzolatti G (2002) Speech listening specifically modulates the excitability of tongue muscles: a TMS study. Eur J Neurosci 15:399–402CrossRefPubMedGoogle Scholar
  9. Filipovic SR, Jahanshahi M, Rothwell JC (1999) Cortical potentials related to decision-making: comparison of two types of go/no-go decision. Neuroreport 10:3583–3587PubMedGoogle Scholar
  10. Filipovic SR, Jahanshahi M, Rothwell JC (2001) Uncoupling of contingent negative variation and alpha band event-related desynchronization in a go/no-go task. Clin Neurophysiol 112:1307–1315CrossRefPubMedGoogle Scholar
  11. Goldman-Rakic P (1996) Prefrontal cortex revisited: a multiple memory domain model of human cognition. In: Caminiti R, Hoffman KP, Lacquaniti F, Altman J (eds) Vision and movement mechanisms in the cerebral cortex. HFSP, StrasbourgGoogle Scholar
  12. Gross CG (1973) Visual functions of inferotemporal cortex. In: Jung R (ed) Handbook of sensory physiology, vol III, part 3B. Springer, Berlin, pp 451–482Google Scholar
  13. Hari R, Forss N, Avikainen S et al. (1998) Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc Natl Acad Sci USA 95:15061–15065CrossRefPubMedGoogle Scholar
  14. Hashimoto R, Rothwell JC (1999) Dynamic changes in corticospinal excitability during motor imagery. Exp Brain Res 125:75–81CrossRefPubMedGoogle Scholar
  15. Howard D (1997) Language in the human brain. In: Rugg M (ed) Cognitive Neurosciences. Psychology, Hove, UKGoogle Scholar
  16. Izumi S, Findley TW, Ikai T et al. (1995) Facilitatory effects of thinking about movement on motor-evoked potential transcranial magnetic stimulation of the brain. Am J Phys Med Rehab 74:207–213Google Scholar
  17. Jahanshahi M, Rothwell JC (2000) Transcranial magnetic stimulation studies of cognition: an emerging field. Exp Brain Res 131:1–9PubMedGoogle Scholar
  18. Kawashima R, Kazunori S, Ryoi G et al. (1998) The role of the inferior temporal cortex for visual pattern discrimination—a PET study. Neuroreport 9:1581–1586PubMedGoogle Scholar
  19. Lemon RN, Johansson RS, Westling G (1995) Cortiocospinal control during reach, grasp, and precision lift in man. J Neurosci 15: 6145–6156PubMedGoogle Scholar
  20. Liberman AM, Whalen DH (2000) On the relation of speech to language. Trends Cogn Neurosci 4:187–196CrossRefGoogle Scholar
  21. Lin K-L, Kobayashi M, Pascual-Leone A (2002) Effects of musical training on speech-induced modulation in corticospinal excitability. Neuroreport 13: 899–902PubMedGoogle Scholar
  22. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedGoogle Scholar
  23. Pesenti M, Thioux M, Seron X, De Volder A (2000) Neuroanatomical substrates of arabic number processing, numerical comparison, and simple addition: a PET study. J Cogn Neurosci 12:461–479CrossRefPubMedGoogle Scholar
  24. Polk TA, Stallcup M, Aguirre GK et al. (2002) Neural specialization for letter recognition. J Cogn Neurosci 14:145–159CrossRefPubMedGoogle Scholar
  25. Puce A, Allison T, Asgari M, Gore JC, McCarthy G (1996) Differential sensitivity of human visual cortex to faces, letterstrings, and textures: a functional magnetic resonance imaging study. J Neurosci 16:5205–5215PubMedGoogle Scholar
  26. Raij T (1999) Patterns of brain activity during visual imagery of letters. J Cogn Neurosci 11:282–299CrossRefPubMedGoogle Scholar
  27. Rickard TC, Romero SG, Basso G et al. (2000) The calculating brain: an fMRI study. Neuropsychologia 38:325–335CrossRefPubMedGoogle Scholar
  28. Rizzolatti G, Arbib MA (1998) Language within our grasp. Trends Neurosci 21:188–194PubMedGoogle Scholar
  29. Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996) Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res 3:131–141Google Scholar
  30. Springer SP, Deutch G (1998) Left brain—right brain: perspectives from cognitive neuroscience, 5th edn. Freeman, New YorkGoogle Scholar
  31. Stephan KM, Fink GR, Passingham RE et al. (1995) Functional anatomy of the mental representation of upper extremity movements in healthy subjects. J Neurophysiol 73:373–386PubMedGoogle Scholar
  32. Strafella AP, Paus T (1999) Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport 11:2289–2292Google Scholar
  33. Tanaka K (1996) Inferotemporal cortex and object recognition. In: Caminiti R., Hoffman KP, Lacquaniti F, Altman J (eds) Vision and movement, mechanisms in the cerebral cortex. HFSP, StrasbourgGoogle Scholar
  34. Tarkiainen A, Cornelissen PL, Salmelin R (1999) Dynamics of visual feature analysis and object level processing in face versus letter-string perception. Brain 125:1125–1136CrossRefGoogle Scholar
  35. Tokimura H, Tokimura Y, Oliviero A, Asakura T, Rothwell JC (1996) Speech induced changes in cortical excitability. Ann Neurol 40:32–37Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • I. Papathanasiou
    • 1
    • 2
    • 3
  • S. R. Filipović
    • 1
    • 2
    • 4
  • R. Whurr
    • 1
    • 2
  • J. C. Rothwell
    • 1
    • 2
  • M. Jahanshahi
    • 1
    • 2
  1. 1.Sobell Department of Motor Neuroscience and Movement Disorders, Institute of NeurologyUniversity College LondonUK
  2. 2.The National Hospital for Neurology and NeurosurgeryLondonUK
  3. 3.Department of Speech and Language TherapyTechnological Educational Institute of PatrasGreece
  4. 4.Burden Neurological InstituteFrenchay HospitalBristolUK

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