Advertisement

Experimental Brain Research

, Volume 160, Issue 1, pp 129–140 | Cite as

Transcranial magnetic stimulation in the visual system. II. Characterization of induced phosphenes and scotomas

  • Thomas KammerEmail author
  • Klaas Puls
  • Michael Erb
  • Wolfgang Grodd
Research Article

Abstract

Transcranial magnetic stimulation (TMS) induces phosphenes and disrupts visual perception when applied over the occipital pole. Both the underlying mechanisms and the brain structures involved are still unclear. In the first part of this study we show that the masking effect of TMS differs to masking by light in terms of the psychometric function. Here we investigate the emergence of phosphenes in relation to perimetric measurements. The coil positions were measured with a stereotactic positioning device, and stimulation sites were characterized in four subjects on the basis of individual retinotopic maps measured by with functional magnetic resonance imaging. Phosphene thresholds were found to lie a factor of 0.59 below the stimulation intensities required to induce visual masking. They covered the segments in the visual field where visual suppression occurred with higher stimulation intensity. Both phosphenes and transient scotomas were found in the lower visual field in the quadrant contralateral to the stimulated hemisphere. They could be evoked from a large area over the occipital pole. Phosphene contours and texture remained quite stable with different coil positions over one hemisphere and did not change with the retinotopy of the different visual areas on which the coil was focused. They cannot be related exclusively to a certain functionally defined visual area. It is most likely that both the optic radiation close to its termination in the dorsal parts of V1 and back-projecting fibers from V2 and V3 back to V1 generate phosphenes and scotomas.

Keywords

Retinotopic mapping Functional magnetic resonance imaging Magnetic stimulation sites Static perimetry Visual masking 

Notes

Acknowledgements

We thank Sandra Beck, Hans-Günther Nusseck, and Kuno Kirschfeld, for support and for many fruitful discussions.

References

  1. Afra J, Mascia A, Gerard P, Maertens de Noordhout A, Schoenen J (1998) Interictal cortical excitability in migraine—a study using transcranial magnetic stimulation of motor and visual cortices. Ann Neurol 44:209–215Google Scholar
  2. Amassian VE, Cracco RQ, Maccabee PJ (1989) Focal stimulation of human cerebral cortex with the magnetic coil: a comparison with electrical stimulation. Electroencephalogr Clin Neurophysiol 74:401–416CrossRefGoogle Scholar
  3. Amassian VE, Eberle L, Maccabee PJ, Cracco RQ (1992) Modelling magnetic coil excitation of human cerebral cortex with a peripheral nerve immersed in a brain-shaped volume conductor: the significance of fiber bending in excitation. Electroencephalogr Clin Neurophysiol 85:291–301CrossRefPubMedGoogle Scholar
  4. Amassian VE, Maccabee PJ, Cracco RQ, Cracco JB, Somasundaram M, Rothwell JC, Eberle L, Henry K, Rudell AP (1994) The polarity of the induced electric field influences magnetic coil inhibition of human visual cortex: implications for the site of excitation. Electroencephalogr Clin Neurophysiol 93:21–26CrossRefPubMedGoogle Scholar
  5. Amunts K, Malikovic A, Mohlberg H, Schormann T, Zilles K (2000) Brodmann’s areas 17 and 18 brought into stereotaxic space—where and how variable? Neuroimage 11:66–84CrossRefPubMedGoogle Scholar
  6. Aurora SK, Ahmad BK, Welch KMA, Bhardhwaj P, Ramadan NM (1998) Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology 50:1111–1114Google Scholar
  7. Beckers G, Hömberg V (1991) Impairment of visual perception and visual short term memory scanning by transcranial magnetic stimulation of occipital cortex. Exp Brain Res 87:421–432PubMedGoogle Scholar
  8. Beckers G, Zeki S (1995) The consequences of inactivating areas V1 and V5 on visual motion perception. Brain 118:49–60PubMedGoogle Scholar
  9. Bohotin V, Fumal A, Vandenheede M, Gerard P, Bohotin C, de Noordhout AM, Schoenen J (2002) Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. Brain 125:912–922CrossRefPubMedGoogle Scholar
  10. Boroojerdi B, Meister IG, Foltys H, Sparing R, Cohen LG, Töpper R (2002) Visual and motor cortex excitability: a transcranial magnetic stimulation study. Clin Neurophysiol 113:1501–1504CrossRefPubMedGoogle Scholar
  11. Brindley GS, Donaldson PE, Falconer MA, Rushton DN (1972) The extent of the region of occipital cortex that when stimulated gives phosphenes fixed in the visual field. J Physiol (Lond) 225:57P–58PGoogle Scholar
  12. Corthout E, Uttl B, Walsh V, Hallett M, Cowey A (1999) Timing of activity in early visual cortex as revealed by transcranial magnetic stimulation. Neuroreport 10:2631–2634PubMedGoogle Scholar
  13. Corthout E, Uttl B, Juan CH, Hallett M, Cowey A (2000) Suppression of vision by transcranial magnetic stimulation: a third mechanism. Neuroreport 11:2345–2349PubMedGoogle Scholar
  14. Cowey A, Walsh V (2000) Magnetically induced phosphenes in sighted, blind and blindsighted observers. Neuroreport 11:3269–3273PubMedGoogle Scholar
  15. Epstein CM, Zangaladze A (1996) Magnetic coil suppression of extrafoveal visual perception using disappearance targets. J Clin Neurophysiol 13:242–246CrossRefPubMedGoogle Scholar
  16. Epstein CM, Schwartzberg DG, Davey KR, Sudderth DB (1990) Localizing the site of magnetic brain stimulation in humans. Neurology 40:666–670Google Scholar
  17. Epstein CM, Verson R, Zangaladze A (1996) Magnetic coil suppression of visual perception at an extracalcarine site. J Clin Neurophysiol 13:247–252CrossRefPubMedGoogle Scholar
  18. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1:1–47PubMedGoogle Scholar
  19. Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257–262CrossRefPubMedGoogle Scholar
  20. Goebel R, Khorramsefat D, Muckli L, Hacker H, Singer W (1998) The constructive nature of vision—direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery. Eur J Neurosci 10:1563–1573CrossRefPubMedGoogle Scholar
  21. Gothe J, Brandt SA, Irlbacher K, Roricht S, Sabel BA, Meyer BU (2002) Changes in visual cortex excitability in blind subjects as demonstrated by transcranial magnetic stimulation. Brain 125:479–490CrossRefPubMedGoogle Scholar
  22. Gregory RL (1970) The intelligent eye. McGraw-Hill, New YorkGoogle Scholar
  23. Hasnain MK, Fox PT, Woldorff MG (1998) Intersubject variability of functional areas in the human visual cortex. Hum Brain Mapp 6:301–315CrossRefPubMedGoogle Scholar
  24. Hupe JM, James AC, Payne BR, Lomber SG, Girard P, Bullier J (1998) Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons. Nature 394:784–787CrossRefPubMedGoogle Scholar
  25. Ilmoniemi RJ, Ruohonen J, Karhu J (1999) Transcranial magnetic stimulation—a new tool for functional imaging of the brain. Crit Rev Biomed Eng 27:241–284PubMedGoogle Scholar
  26. Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol (Lond) 466:521–534Google Scholar
  27. Jalinous R (1991) Technical and practical aspects of magnetic nerve stimulation. J Clin Neurophysiol 8:10–25PubMedGoogle Scholar
  28. Kamitani Y, Shimojo S (1999) Manifestation of scotomas created by transcranial magnetic stimulation of human visual cortex. Nat Neurosci 2:767–771CrossRefPubMedGoogle Scholar
  29. Kammer T (1999) Phosphenes and transient scotomas induced by magnetic stimulation of the occipital lobe: their topographic relationship. Neuropsychologia 37:191–198CrossRefPubMedGoogle Scholar
  30. Kammer T, Beck S (2002) Phosphene thresholds evoked by transcranial magnetic stimulation are insensitive to short-lasting variations in ambient light. Exp Brain Res 145:407–410CrossRefPubMedGoogle Scholar
  31. Kammer T, Nusseck HG (1998) Are recognition deficits following occipital lobe TMS explained by raised detection thresholds? Neuropsychologia 36:1161–1166CrossRefPubMedGoogle Scholar
  32. Kammer T, Erb M, Beck S, Grodd W (2000) Multimodal mapping of the visual cortex: comparison of functional MRI and stereotactic TMS. Eur J Neurosci 12 [Suppl] 11:192Google Scholar
  33. Kammer T, Beck S, Erb M, Grodd W (2001a) The influence of current direction on phosphene thresholds evoked by transcranial magnetic stimulation. Clin Neurophysiol 112:2015–2021CrossRefPubMedGoogle Scholar
  34. Kammer T, Beck S, Thielscher A, Laubis-Herrmann U, Topka H (2001b) Motor thresholds in humans. A transcranial magnetic stimulation study comparing different pulseforms, current directions and stimulator types. Clin Neurophysiol 112:250–258CrossRefPubMedGoogle Scholar
  35. Kammer T, Puls K, Strasburger H, Hill NJ, Wichmann FA (2004) TMS in the visual system. I. The psychophysics of visual suppression. Exp Brain Res ( http://dx.doi.org/10.1007/s00221-004-1991-1)
  36. Kastner S, Paul I, Ziemann U (1998) Transient visual field defects induced by transcranial magnetic stimulation over the occipital lobe. Exp Brain Res 118:19–26CrossRefPubMedGoogle Scholar
  37. Kosslyn SM, Pascual-Leone A, Felician O, Camposano S, Keenan JP, Thompson WL, Ganis G, Sukel KE, Alpert NM (1999) The role of area 17 in visual imagery: convergent evidence from PET and rTMS. Science 284:167–170CrossRefPubMedGoogle Scholar
  38. Lee HW, Hong SB, Seo DW, Tae WS, Hong SC (2000) Mapping of functional organization in human visual cortex—electrical cortical stimulation. Neurology 54:849–854Google Scholar
  39. Maccabee PJ, Amassian VE, Eberle LP, Cracco RQ (1993) Magnetic coil stimulation of straight and bent amphibian and mammalian peripheral nerve in vitro: locus of excitation. J Physiol (Lond) 460:201–219Google Scholar
  40. Marg E, Rudiak D (1994) Phosphenes induced by magnetic stimulation over the occipital brain: description and probable site of stimulation. Optom Vis Sci 71:301–311PubMedGoogle Scholar
  41. Meyer BU, Diehl RR, Steinmetz H, Britton TC, Benecke R (1991) Magnetic stimuli applied over motor cortex and visual cortex: influence of coil position and field polarity on motor responses, phosphenes, and eye movements. Electroencephalogr Clin Neurophysiol Suppl 43:121–134PubMedGoogle Scholar
  42. Pascual-Leone A, Walsh V (2001) Fast backprojections from the motion to the primary visual area necessary for visual awareness. Science 292:510–512PubMedGoogle Scholar
  43. Penfield W, Rasmussen T (1950) The cerebral cortex of man: a clinical study of localization and function. Macmillan, New YorkGoogle Scholar
  44. Potts GF, Gugino LD, Leventon ME, Grimson WEL, Kikinis R, Cote W, Alexander E, Anderson JE, Ettinger GJ, Aglio LS, Shenton ME (1998) Visual hemifield mapping using transcranial magnetic stimulation coregistered with cortical surfaces derived from magnetic resonance images. J Clin Neurophysiol 15:344–350CrossRefPubMedGoogle Scholar
  45. Ray PG, Meador KJ, Epstein CM, Loring DW, Day LJ (1998) Magnetic stimulation of visual cortex: factors influencing the perception of phosphenes. J Clin Neurophysiol 15:351–357CrossRefPubMedGoogle Scholar
  46. Rothwell JC (1997) Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 74:113–122CrossRefPubMedGoogle Scholar
  47. Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RBH (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889–893PubMedGoogle Scholar
  48. Sparing R, Mottaghy FM, Ganis G, Thompson WL, Töpper R, Kosslyn SM, Pascual-Leone A (2002) Visual cortex excitability increases during visual mental imagery—a TMS study in healthy human subjects. Brain Res 938:92–97CrossRefPubMedGoogle Scholar
  49. Stewart LM, Walsh V, Rothwell JC (2001) Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study. Neuropsychologia 39:415–419CrossRefPubMedGoogle Scholar
  50. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, StuttgartGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Thomas Kammer
    • 1
    • 2
    Email author
  • Klaas Puls
    • 2
  • Michael Erb
    • 3
  • Wolfgang Grodd
    • 3
  1. 1.Department of PsychiatryUniversity of UlmUlmGermany
  2. 2.Department of NeurobiologyMax Planck Institute for Biological CyberneticsTübingenGermany
  3. 3.Section Exp. MR of CNS, Department of NeuroradiologyUniversity of TübingenTübingenGermany

Personalised recommendations