Experimental Brain Research

, Volume 162, Issue 1, pp 23–34 | Cite as

Perceptual learning of line orientation modifies the effects of transcranial magnetic stimulation of visual cortex

Research Article


Perceptual learning may be accompanied by physiological changes in early visual cortex. We used transcranial magnetic stimulation (TMS) to test the postulate that perceptual learning of a visual task initially performed at 60–65% accuracy strengthens visual processing in early visual cortex. Single pulse TMS was delivered to human occipital cortex at time delays of 70–154 ms after the onset of an odd-element, line orientation discrimination task. When TMS was delivered at a delay of 84 ms or later the accuracy of visual discrimination was transiently degraded in ten subjects. As visual performance in control trials without TMS improved with training, the absolute magnitude of TMS suppression of performance decreased in parallel. This result occurred both when TMS was delivered to broad areas of occipital cortex and when TMS was optimally delivered to early occipital cortex. No change in TMS suppression was observed when three new subjects were given feedback during an odd-element task that did not require substantial perceptual learning. Thus, perceptual learning improved visual performance and reduced TMS suppression of early visual cortex in parallel.


Perceptual learning Transcranial magnetic stimulation Visual cortex Line orientation Human psychophysics 


  1. Adini Y, Sagi D, Tsodyks M (2002) Context-enabled learning in the human visual system. Nature 415:790–793PubMedGoogle Scholar
  2. Ahissar M, Hochstein S (1993) Attentional control of early perceptual learning. Proc Natl Acad Sci USA 90:5718–5722PubMedGoogle Scholar
  3. Ahissar M, Hochstein S (1997) Task difficulty and the specificity of perceptual learning. Nature 387:401–406CrossRefPubMedGoogle Scholar
  4. Ahissar M, Laiwand R, Kozminsky G, Hochstein S (1998) Learning pop-out detection: building representations for conflicting target-distractor relationships. Vision Res 38:3095–3107CrossRefPubMedGoogle Scholar
  5. Amassian VE, Cracco RQ, Maccabee PJ, Cracco JB, Rudell A, Eberle L (1989) Suppression of visual perception by magnetic coil stimulation of human occipital cortex. Electroen Clin Neuro 74:458–462Google Scholar
  6. Amassian VE, Cracco RQ, Maccabee PJ, Cracco JB, Rudell AP, Eberle L (1993) Unmasking human visual perception with the magnetic coil and its relationship to hemispheric asymmetry. Brain Res 605:312–316CrossRefPubMedGoogle Scholar
  7. Anand S, Hotson J (2002) Transcranial magnetic stimulation: Neurophysiological applications and safety. Brain Cognition 50:366–386CrossRefGoogle Scholar
  8. Anand S, Olson JD, Hotson JR (1998) Tracing the timing of human analysis of motion and chromatic signals from occipital to temporo-parieto-occipital cortex: a transcranial magnetic stimulation study. Vision Res 38:2619–2627CrossRefPubMedGoogle Scholar
  9. Ball K, Sekuler R (1982) A specific and enduring improvement in visual motion discrimination. Science 218:697–698PubMedGoogle Scholar
  10. Boroojerdi B, Bushara KO, Corwell B, Immisch I, Battaglia F, Muellbacher W, Cohen LG (2000) Enhanced excitability of the human visual cortex induced by short-term light deprivation. Cereb Cortex 10:529–534CrossRefPubMedGoogle Scholar
  11. Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436PubMedGoogle Scholar
  12. Brasil-Neto JP, McShane LM, Fuhr P, Hallett M, Cohen LG (1992) Topographic mapping of the human motor cortex with magnetic stimulation: factors affecting accuracy and reproducibility. Electroen Clin Neuro 85:9-16Google Scholar
  13. Campana G, Cowey A, Walsh V (2002) Priming of motion direction and area V5/MT: a test of perceptual memory. Cereb Cortex 12:663–669CrossRefPubMedGoogle Scholar
  14. Chino YM, Kaas JH, Smith EL 3rd, Langston AL, Cheng H (1992) Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina. Vision Res 32:789–796CrossRefPubMedGoogle Scholar
  15. Cohen LG, Roth BJ, Nilsson J, Dang N, Panizza M, Bandinelli S, Friauf W, Hallett M (1990) Effects of coil design on delivery of focal magnetic stimulation. Technical considerations. Electroen Clin Neuro 75:350–357CrossRefGoogle Scholar
  16. Corthout E, Uttl B, Walsh V, Hallett M, Cowey A (2000) Plasticity revealed by transcranial magnetic stimulation of early visual cortex. Neuroreport 11:1565–1569PubMedGoogle Scholar
  17. Crist RE, Kapadia MK, Westheimer G, Gilbert CD (1997) Perceptual learning of spatial localization: specificity for orientation, position and context. J Neurophysiol 78:2889–2894Google Scholar
  18. Crist RE, Li W, Gilbert CD (2001) Learning to see: experience and attention in primary visual cortex. Nat Neurosci 4:519–525PubMedGoogle Scholar
  19. Dosher BA, Lu ZL (1998) Perceptual learning reflects external noise filtering and internal noise reduction through channel reweighting. Proc Natl Acad Sci USA 95:13988–13993CrossRefPubMedGoogle Scholar
  20. Dragoi V, Rivadulla C, Sur M (2001) Foci of orientation plasticity in visual cortex. Nature 411:80–86CrossRefPubMedGoogle Scholar
  21. Eysel UT, Schweigart G (1999) Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex. Cereb Cortex 9:101–109CrossRefPubMedGoogle Scholar
  22. Fahle M, Poggio T (2002) Perceptual Learning. The MIT Press, CambridgeGoogle Scholar
  23. Fahle M, Edelman S, Poggio T (1995) Fast perceptual learning in hyperacuity. Vision Res 35:3003–3013CrossRefPubMedGoogle Scholar
  24. Fendick M, Westheimer G (1983) Effects of practice and the separation of test targets on foveal and peripheral stereoacuity. Vision Res 23:145–150CrossRefPubMedGoogle Scholar
  25. Fiorentini A, Berardi N (1980) Perceptual learning specific for orientation and spatial frequency. Nature 287:43–44PubMedGoogle Scholar
  26. Furmanski CS, Engel SA (2000) Perceptual learning in object recognition: object specificity and size invariance. Vision Res 40:473–484CrossRefPubMedGoogle Scholar
  27. Furmanski CS, Engel SA (2002) Perceptual learning leads to increases in V1 activity. Soc Neurosci Abstr Viewer 721.3Google Scholar
  28. Ghose GM, Yang T, Maunsell JH (2002) Physiological correlates of perceptual learning in monkey V1 and V2. J Neurophysiol 87:1867–1888Google Scholar
  29. Gilbert CD, Wiesel TN (1992) Receptive field dynamics in adult primary visual cortex. Nature 356:150–152CrossRefPubMedGoogle Scholar
  30. Godde B, Sprengler F, Dinse HR (1996) Associative pairing of tactile stimulation induces somatosensory cortical reorganization in rats and humans. Neuroreport 8:281–285PubMedGoogle Scholar
  31. Godde B, Stauffenberg B, Spengler F, Dinse HR (2000) Tactile coactivation-induced changes in spatial discrimination performance. J Neurosci 20:1597–1604PubMedGoogle Scholar
  32. Grafman J (2002) The use of transcranial magnetic stimulation in learning and memory research. In: Pascual-Leone A, Davey N, Rothwell J, Wassermann E, Puri B (eds) Handbook of transcranial magnetic stimulation. Arnold, London, pp 303–313Google Scholar
  33. Hochstein S, Ahissar M (2002) View from the top: hierarchies and reverse hierarchies in the visual system. Neuron 36:791–804CrossRefPubMedGoogle Scholar
  34. Hotson JR, Anand S (1999) The selectivity and timing of motion processing in human temporo-parieto-occipital and occipital cortex: a transcranial magnetic stimulation study. Neuropsychologia 37:169–179Google Scholar
  35. Hotson J, Braun D, Herzberg W, Boman D (1994) Transcranial magnetic stimulation of extrastriate cortex degrades human motion direction discrimination. Vision Res 34:2115–2123CrossRefPubMedGoogle Scholar
  36. Juan CH, Walsh V (2003) Feedback to V1: a reverse hierarchy in vision. Exp Brain Res 150:259–263PubMedGoogle Scholar
  37. Kaas JH, Krubitzer LA, Chino YM, Langston AL, Polley EH, Blair N (1990) Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248:229–231PubMedGoogle Scholar
  38. Kammer T (1999) Phosphenes and transient scotomas induced by magnetic stimulation of the occipital lobe: their topographic relationship. Neuropsychologia 37:191–198CrossRefPubMedGoogle Scholar
  39. Kapadia MK, Ito M, Gilbert CD, Westheimer G (1995) Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys. Neuron 15:843–856CrossRefPubMedGoogle Scholar
  40. Karni A, Sagi D (1991) Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. Proc Natl Acad Sci USA 88:4966–4970PubMedGoogle Scholar
  41. Karni A, Weisberg F, Lalonde F, Ungerleider L (1995) An fMRI study of human visual cortex plasticity. Soc Neurosci Abstr 21:276Google Scholar
  42. Kastner S, Demmer I, Ziemann U (1998) Transient visual field defects induced by transcranial magnetic stimulation over human occipital pole. Exp Brain Res 118:19–26CrossRefPubMedGoogle Scholar
  43. Klaes C, Ragert P, Jancke DE, Tegenthoff M, Dinse H (2003) rTMS induced improvement of human orientation discrimination. Soc Neurosci Abstr Viewer 911:22Google Scholar
  44. Kobatake E, Wang G, Tanaka K (1998) Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. J Neurophysiol 80:324–330Google Scholar
  45. Lee TS, Yang CF, Romero RD, Mumford D (2002) Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency. Nat Neurosci 5:589–597CrossRefPubMedGoogle Scholar
  46. McKee SP, Westheimer G (1978) Improvement in vernier acuity with practice. Percept Psychophys 24:258–262PubMedGoogle Scholar
  47. Neary K, Gee B, Anand S, Hotson J (2001) Does perceptual learning change the effect of transcranial magnetic stimulation (TMS) on visual cortex? Soc Neurosci Abstr Viewer 619:54Google Scholar
  48. Neary K, Anand S, Gee B, Hotson J (2003) Perceptual learning increases the strength of early visual processing as measured by increased resistance to transcranial magnetic stimulation. Invest Ophthalmol Vis Sci 44:4101Google Scholar
  49. 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
  50. Pleger B, Dinse HR, Ragert P, Schwenkreis P, Malin JP, Tegenthoff M (2001) Shifts in cortical representations predict human discrimination improvement. Proc Natl Acad Sci USA 98:12255–12260CrossRefPubMedGoogle Scholar
  51. Polat U, Sagi D (1994) Spatial interactions in human vision: from near to far via experience-dependent cascades of connections. Proc Natl Acad Sci USA 91:1206–1209PubMedGoogle Scholar
  52. Ragert P, Becker M, Tegenthoff M, Pleger B, Dinse HR (2004) Sustained increase of somatosensoy cortex excitability by 5 Hz repetitive transcranial magnetic stimulation studied by paired median nerve stimulation in humans. Neurosci Lett 356:91–94CrossRefPubMedGoogle Scholar
  53. Rainer G, Lee H, Logothetis NK (2004) The effect of learning on the function of monkey exstrastriate visual cortex. PLoS Bio 2:E44Google Scholar
  54. Ramachandran VS (1976) Learning-like phenomena in stereopsis. Nature 262: 382–384PubMedGoogle Scholar
  55. Recanzone GH, Merzenich MM, Jenkins WM, Grajski KA, Dinse HR (1992a) Topographical reorganization of the hand representation in cortical area 3b of owl monkeys trained in a frequency-discrimination task. J Neurophysiol 67:1031–1056Google Scholar
  56. Recanzone GH, Merzenich MM, Schreiner CE (1992b) Changes in the distributed temporal response properties of S1 cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. J Neurophysiol 67:1071–1091Google Scholar
  57. Roth BJ, Saypol JM, Hallett M, Cohen LG (1991) A theoretical calculation of the electric field induced in the cortex during magnetic stimulation. Electroen Clin Neuro 81:47–56Google Scholar
  58. Schiltz C, Bodart JM, Dubois S, Dejardin S, Michel C, Roucoux A, Crommelinck M, Orban GA (1999) Neuronal mechanisms of perceptual learning: changes in human brain activity with training in orientation discrimination. Neuroimage 9:46–62CrossRefPubMedGoogle Scholar
  59. Schoups AA, Vogels R, Orban GA (1995) Human perceptual learning in identifying the oblique orientation: retinotopy, orientation specificity and monocularity. J Physiol (Lond) 483.3:797–810Google Scholar
  60. Schoups A, Vogels R, Qian N, Orban G (2001) Practising orientation identification improves orientation coding in V1 neurons. Nature 412:549–553CrossRefPubMedGoogle Scholar
  61. Schweigart G, Eysel UT (2002) Activity-dependent receptive field changes in the surround of adult cat visual cortex lesions. Eur J Neurosci 15:1585–1596CrossRefPubMedGoogle Scholar
  62. Teich AF, Qian N (2003) Learning and adaptation in a recurrent model of V1 orientation selectivity. J Neurophysiol 89:2086–2100Google Scholar
  63. Walsh V, Ashbridge E, Cowey A (1998) Cortical plasticity in perceptual learning demonstrated by transcranial magnetic stimulation. Neuropsychologia 36:363–367Google Scholar
  64. Watanabe T, Nanez JE Sr, Koyama S, Mukai I, Liederman J, Saski Y (2002) Greater plasticity in lower-level than higher-level visual motion processing in a passive perceptual learning task. Nat Neurosci 5:1003–1009CrossRefPubMedGoogle Scholar
  65. Werhahn KJ, Taylor J, Ridding M, Meyer BU, Rothwell JC (1996) Effect of trancranial magnetic stimulation over the cerebellum on the excitability of human motor cortex. Electroen Clin Neuro 101:58–66CrossRefGoogle Scholar
  66. Yang T, Maunsell JH (2004) The effect of perceptual learning on neuronal responses in monkey visual area V4. J Neurosci 24:1617–1626CrossRefPubMedGoogle Scholar
  67. Zohary E, Celebrini C, Britten KH, Newsome WT (1994) Neuronal plasticity that underlies improvement in perceptual performance. Science 263:1289–1292PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.California Institute for Medical ResearchSan JoseUSA
  2. 2.Department of Biological SciencesSan Jose State UniversitySan JoseUSA
  3. 3.Department of Neurology & Neurological SciencesStanford University and Santa Clara Valley Medical CenterStanford and San JoseUSA

Personalised recommendations