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

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Abstract

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.

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References

  • Adini Y, Sagi D, Tsodyks M (2002) Context-enabled learning in the human visual system. Nature 415:790–793

    PubMed  Google Scholar 

  • Ahissar M, Hochstein S (1993) Attentional control of early perceptual learning. Proc Natl Acad Sci USA 90:5718–5722

    CAS  PubMed  Google Scholar 

  • Ahissar M, Hochstein S (1997) Task difficulty and the specificity of perceptual learning. Nature 387:401–406

    Article  CAS  PubMed  Google Scholar 

  • Ahissar M, Laiwand R, Kozminsky G, Hochstein S (1998) Learning pop-out detection: building representations for conflicting target-distractor relationships. Vision Res 38:3095–3107

    Article  CAS  PubMed  Google Scholar 

  • 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 74:458–462

    CAS  Google Scholar 

  • 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 605:312–316

    Article  CAS  PubMed  Google Scholar 

  • Anand S, Hotson J (2002) Transcranial magnetic stimulation: Neurophysiological applications and safety. Brain Cognition 50:366–386

    Article  Google Scholar 

  • 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 38:2619–2627

    Article  CAS  PubMed  Google Scholar 

  • Ball K, Sekuler R (1982) A specific and enduring improvement in visual motion discrimination. Science 218:697–698

    CAS  PubMed  Google Scholar 

  • 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 10:529–534

    Article  CAS  PubMed  Google Scholar 

  • Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436

    CAS  PubMed  Google Scholar 

  • 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 85:9-16

    CAS  Google Scholar 

  • Campana G, Cowey A, Walsh V (2002) Priming of motion direction and area V5/MT: a test of perceptual memory. Cereb Cortex 12:663–669

    Article  PubMed  Google Scholar 

  • 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 32:789–796

    Article  CAS  PubMed  Google Scholar 

  • 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 75:350–357

    Article  CAS  Google Scholar 

  • Corthout E, Uttl B, Walsh V, Hallett M, Cowey A (2000) Plasticity revealed by transcranial magnetic stimulation of early visual cortex. Neuroreport 11:1565–1569

    CAS  PubMed  Google Scholar 

  • Crist RE, Kapadia MK, Westheimer G, Gilbert CD (1997) Perceptual learning of spatial localization: specificity for orientation, position and context. J Neurophysiol 78:2889–2894

    Google Scholar 

  • Crist RE, Li W, Gilbert CD (2001) Learning to see: experience and attention in primary visual cortex. Nat Neurosci 4:519–525

    CAS  PubMed  Google Scholar 

  • Dosher BA, Lu ZL (1998) Perceptual learning reflects external noise filtering and internal noise reduction through channel reweighting. Proc Natl Acad Sci USA 95:13988–13993

    Article  CAS  PubMed  Google Scholar 

  • Dragoi V, Rivadulla C, Sur M (2001) Foci of orientation plasticity in visual cortex. Nature 411:80–86

    Article  CAS  PubMed  Google Scholar 

  • Eysel UT, Schweigart G (1999) Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex. Cereb Cortex 9:101–109

    Article  CAS  PubMed  Google Scholar 

  • Fahle M, Poggio T (2002) Perceptual Learning. The MIT Press, Cambridge

  • Fahle M, Edelman S, Poggio T (1995) Fast perceptual learning in hyperacuity. Vision Res 35:3003–3013

    Article  CAS  PubMed  Google Scholar 

  • Fendick M, Westheimer G (1983) Effects of practice and the separation of test targets on foveal and peripheral stereoacuity. Vision Res 23:145–150

    Article  CAS  PubMed  Google Scholar 

  • Fiorentini A, Berardi N (1980) Perceptual learning specific for orientation and spatial frequency. Nature 287:43–44

    CAS  PubMed  Google Scholar 

  • Furmanski CS, Engel SA (2000) Perceptual learning in object recognition: object specificity and size invariance. Vision Res 40:473–484

    Article  CAS  PubMed  Google Scholar 

  • Furmanski CS, Engel SA (2002) Perceptual learning leads to increases in V1 activity. Soc Neurosci Abstr Viewer 721.3

  • Ghose GM, Yang T, Maunsell JH (2002) Physiological correlates of perceptual learning in monkey V1 and V2. J Neurophysiol 87:1867–1888

    Google Scholar 

  • Gilbert CD, Wiesel TN (1992) Receptive field dynamics in adult primary visual cortex. Nature 356:150–152

    Article  CAS  PubMed  Google Scholar 

  • Godde B, Sprengler F, Dinse HR (1996) Associative pairing of tactile stimulation induces somatosensory cortical reorganization in rats and humans. Neuroreport 8:281–285

    CAS  PubMed  Google Scholar 

  • Godde B, Stauffenberg B, Spengler F, Dinse HR (2000) Tactile coactivation-induced changes in spatial discrimination performance. J Neurosci 20:1597–1604

    CAS  PubMed  Google Scholar 

  • 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 303–313

  • Hochstein S, Ahissar M (2002) View from the top: hierarchies and reverse hierarchies in the visual system. Neuron 36:791–804

    Article  PubMed  Google Scholar 

  • 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 37:169–179

    Google Scholar 

  • Hotson J, Braun D, Herzberg W, Boman D (1994) Transcranial magnetic stimulation of extrastriate cortex degrades human motion direction discrimination. Vision Res 34:2115–2123

    Article  CAS  PubMed  Google Scholar 

  • Juan CH, Walsh V (2003) Feedback to V1: a reverse hierarchy in vision. Exp Brain Res 150:259–263

    PubMed  Google Scholar 

  • 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 248:229–231

    CAS  PubMed  Google Scholar 

  • Kammer T (1999) Phosphenes and transient scotomas induced by magnetic stimulation of the occipital lobe: their topographic relationship. Neuropsychologia 37:191–198

    Article  CAS  PubMed  Google Scholar 

  • 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 15:843–856

    Article  CAS  PubMed  Google Scholar 

  • Karni A, Sagi D (1991) Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. Proc Natl Acad Sci USA 88:4966–4970

    CAS  PubMed  Google Scholar 

  • Karni A, Weisberg F, Lalonde F, Ungerleider L (1995) An fMRI study of human visual cortex plasticity. Soc Neurosci Abstr 21:276

    Google Scholar 

  • Kastner S, Demmer I, Ziemann U (1998) Transient visual field defects induced by transcranial magnetic stimulation over human occipital pole. Exp Brain Res 118:19–26

    Article  CAS  PubMed  Google Scholar 

  • Klaes C, Ragert P, Jancke DE, Tegenthoff M, Dinse H (2003) rTMS induced improvement of human orientation discrimination. Soc Neurosci Abstr Viewer 911:22

    Google Scholar 

  • Kobatake E, Wang G, Tanaka K (1998) Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. J Neurophysiol 80:324–330

    Google Scholar 

  • 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 5:589–597

    Article  CAS  PubMed  Google Scholar 

  • McKee SP, Westheimer G (1978) Improvement in vernier acuity with practice. Percept Psychophys 24:258–262

    CAS  PubMed  Google Scholar 

  • 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 619:54

    Google Scholar 

  • 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 44:4101

    Google Scholar 

  • Pascual-Leone A, Walsh V (2001) Fast backprojections from the motion to the primary visual area necessary for visual awareness. Science 292:510–512

    CAS  PubMed  Google Scholar 

  • 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 98:12255–12260

    Article  CAS  PubMed  Google Scholar 

  • 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 91:1206–1209

    CAS  PubMed  Google Scholar 

  • 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 356:91–94

    Article  CAS  PubMed  Google Scholar 

  • Rainer G, Lee H, Logothetis NK (2004) The effect of learning on the function of monkey exstrastriate visual cortex. PLoS Bio 2:E44

    Google Scholar 

  • Ramachandran VS (1976) Learning-like phenomena in stereopsis. Nature 262: 382–384

    CAS  PubMed  Google Scholar 

  • 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 67:1031–1056

    Google Scholar 

  • 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 67:1071–1091

    Google Scholar 

  • 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 81:47–56

    CAS  Google Scholar 

  • 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 9:46–62

    Article  CAS  PubMed  Google Scholar 

  • Schoups AA, Vogels R, Orban GA (1995) Human perceptual learning in identifying the oblique orientation: retinotopy, orientation specificity and monocularity. J Physiol (Lond) 483.3:797–810

    Google Scholar 

  • Schoups A, Vogels R, Qian N, Orban G (2001) Practising orientation identification improves orientation coding in V1 neurons. Nature 412:549–553

    Article  CAS  PubMed  Google Scholar 

  • Schweigart G, Eysel UT (2002) Activity-dependent receptive field changes in the surround of adult cat visual cortex lesions. Eur J Neurosci 15:1585–1596

    Article  PubMed  Google Scholar 

  • Teich AF, Qian N (2003) Learning and adaptation in a recurrent model of V1 orientation selectivity. J Neurophysiol 89:2086–2100

    Google Scholar 

  • Walsh V, Ashbridge E, Cowey A (1998) Cortical plasticity in perceptual learning demonstrated by transcranial magnetic stimulation. Neuropsychologia 36:363–367

    Google Scholar 

  • 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 5:1003–1009

    Article  CAS  PubMed  Google Scholar 

  • 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 101:58–66

    Article  CAS  Google Scholar 

  • Yang T, Maunsell JH (2004) The effect of perceptual learning on neuronal responses in monkey visual area V4. J Neurosci 24:1617–1626

    Article  PubMed  Google Scholar 

  • Zohary E, Celebrini C, Britten KH, Newsome WT (1994) Neuronal plasticity that underlies improvement in perceptual performance. Science 263:1289–1292

    CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by The Valley Foundation, San Jose, CA, USA (J.R.H.)

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Authors and Affiliations

  1. California Institute for Medical Research, 2260 Clove Drive, San Jose, CA, 95128, USA

    K. Neary & J. R. Hotson

  2. Department of Biological Sciences, San Jose State University, San Jose, CA, USA

    S. Anand

  3. Department of Neurology & Neurological Sciences, Stanford University and Santa Clara Valley Medical Center, Stanford and San Jose, CA, USA

    J. R. Hotson

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  1. K. Neary
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Correspondence to J. R. Hotson.

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Neary, K., Anand, S. & Hotson, J.R. Perceptual learning of line orientation modifies the effects of transcranial magnetic stimulation of visual cortex. Exp Brain Res 162, 23–34 (2005). https://doi.org/10.1007/s00221-004-2117-5

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