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Applying Transcranial Magnetic Stimulation (TMS) Over the Dorsal Visual Pathway Induces Schizophrenia-like Disruption of Perceptual Closure

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Abstract

Perceptual closure ability is postulated to depend upon rapid transmission of magnocellular information to prefrontal cortex via the dorsal stream. In contrast, illusory contour processing requires only local interactions within primary and ventral stream visual regions, such as lateral occipital complex. Schizophrenia is associated with deficits in perceptual closure versus illusory contours processing that is hypothesized to reflect impaired magnocellular/dorsal stream. Perceptual closure and illusory contours performance was evaluated in separate groups of 12 healthy volunteers during no TMS, and during repetitive 10 Hz rTMS stimulation over dorsal stream or vertex (TMS-vertex). Perceptual closure and illusory contours were performed in 11 schizophrenia patients, no TMS was applied in these patients. TMS effects were evaluated with repeated measures ANOVA across treatments. rTMS significantly increased perceptual closure identification thresholds, with significant difference between TMS-dorsal stream and no TMS. TMS-dorsal stream also significantly reduced perceptual closure but not illusory contours accuracy. Schizophrenia patients showed increased perceptual closure identification thresholds relative to controls in the no TMS condition, but similar to controls in the TMS-dorsal stream condition. Conclusions of this study are that magnocellular/dorsal stream input is critical for perceptual closure but not illusory contours performance, supporting both trickledown theories of normal perceptual closure function, and magnocellular/dorsal stream theories of visual dysfunction in schizophrenia.

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References

  • Bar M (2003) A cortical mechanism for triggering top-down facilitation in visual object recognition. J Cogn Neurosci 15(4):600–609

    Article  PubMed  Google Scholar 

  • Bocker KB, van Avermaete JA, van den Berg-Lenssen MM (1994) The international 10-20 system revisited: cartesian and spherical co-ordinates. Brain Topogr 6(3):231–235

    Article  CAS  PubMed  Google Scholar 

  • Butler PD, Martinez A, Foxe JJ, Kim D, Zemon V, Silipo G, Mahoney J, Shpaner M, Jalbrzikowski M, Javitt DC (2007) Subcortical visual dysfunction in schizophrenia drives secondary cortical impairments. Brain 130(Pt 2):417–430

    Article  PubMed  Google Scholar 

  • Cash TF, Deagle EA 3rd (1997) The nature and extent of body-image disturbances in anorexia nervosa and bulimia nervosa: a meta-analysis. Int J Eat Disord 22(2):107–125

    Article  CAS  PubMed  Google Scholar 

  • Chen CM, Lakatos P, Shah AS, Mehta AD, Givre SJ, Javitt DC, Schroeder CE (2007) Functional anatomy and interaction of fast and slow visual pathways in macaque monkeys. Cereb Cortex 17(7):1561–1569

    Article  PubMed  Google Scholar 

  • Chouinard PA, Whitwell RL, Goodale MA (2009) The lateral-occipital and the inferior-frontal cortex play different roles during the naming of visually presented objects. Hum Brain Mapp 30(12):3851–3864

    Article  PubMed  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale

    Google Scholar 

  • Di Russo F, Martinez A, Sereno MI, Pitzalis S, Hillyard SA (2002) Cortical sources of the early components of the visual evoked potential. Hum Brain Mapp 15(2):95–111

    Article  PubMed  Google Scholar 

  • Doniger GM, Foxe JJ, Murray MM, Higgins BA, Snodgrass JG, Schroeder CE, Javitt DC (2000) Activation time course of ventral visual stream object-recognition areas: high density electrical mapping of perceptual closure processes. J Cogn Neurosci 12(4):615–621

    Article  CAS  PubMed  Google Scholar 

  • Doniger GM, Silipo G, Rabinowicz EF, Snodgrass JG, Javitt DC (2001) Impaired sensory processing as a basis for object-recognition deficits in schizophrenia. Am J Psychiatry 158(11):1818–1826

    Article  CAS  PubMed  Google Scholar 

  • Doniger GM, Foxe JJ, Murray MM, Higgins BA, Javitt DC (2002) Impaired visual object recognition and dorsal/ventral stream interaction in schizophrenia. Arch Gen Psychiatry 59(11):1011–1020

    Article  PubMed  Google Scholar 

  • Ellison A, Cowey A (2006) TMS can reveal contrasting functions of the dorsal and ventral visual processing streams. Exp Brain Res 175(4):618–625

    Article  PubMed  Google Scholar 

  • Ellison A, Cowey A (2009) Differential and co-involvement of areas of the temporal and parietal streams in visual tasks. Neuropsychologia 47(6):1609–1614

    Article  PubMed  Google Scholar 

  • Ellison A, Battelli L, Cowey A, Walsh V (2003) The effect of expectation on facilitation of colour/form conjunction tasks by TMS over area V5. Neuropsychologia 41(13):1794–1801

    Article  PubMed  Google Scholar 

  • Fecteau S, Walsh V (2012) Introduction: Brain stimulation in cognitive neuroscience. Brain Stimul 5(2):61–62

    Article  PubMed  Google Scholar 

  • Fenske MJ, Aminoff E, Gronau N, Bar M (2006) Top-down facilitation of visual object recognition: object-based and context-based contributions. Prog Brain Res 155:3–21

    Article  PubMed  Google Scholar 

  • Foxe JJ, Doniger GM, Javitt DC (2001) Early visual processing deficits in schizophrenia: impaired P1 generation revealed by high-density electrical mapping. NeuroReport 12(17):3815–3820

    Article  CAS  PubMed  Google Scholar 

  • Foxe JJ, Murray MM, Javitt DC (2005) Filling-in in schizophrenia: a high-density electrical mapping and source-analysis investigation of illusory contour processing. Cereb Cortex 15(12):1914–1927

    Article  PubMed  Google Scholar 

  • Grosof DH, Shapley RM, Hawken MJ (1993) Macaque V1 neurons can signal ‘illusory’ contours. Nature 365(6446):550–552

    Article  CAS  PubMed  Google Scholar 

  • Halgren E, Mendola J, Chong CD, Dale AM (2003) Cortical activation to illusory shapes as measured with magnetoencephalography. Neuroimage 18(4):1001–1009

    Article  PubMed  Google Scholar 

  • Javitt DC (2009) When doors of perception close: bottom-up models of disrupted cognition in schizophrenia. Annu Rev Clin Psychol 5:249–275

    Article  PubMed  PubMed Central  Google Scholar 

  • Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13(2):261–276

    Article  CAS  PubMed  Google Scholar 

  • Keane BP, Joseph J, Silverstein SM (2014) Late, not early, stages of Kanizsa shape perception are compromised in schizophrenia. Neuropsychologia 56:302–311

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim D, Zemon V, Saperstein A, Butler PD, Javitt DC (2005) Dysfunction of early-stage visual processing in schizophrenia: harmonic analysis. Schizophr Res 76(1):55–65

    Article  PubMed  Google Scholar 

  • Kim D, Wylie G, Pasternak R, Butler PD, Javitt DC (2006) Magnocellular contributions to impaired motion processing in schizophrenia. Schizophr Res 82(1):1–8

    Article  CAS  PubMed  Google Scholar 

  • Knebel JF, Javitt DC, Murray MM (2011) Impaired early visual response modulations to spatial information in chronic schizophrenia. Psychiatry Res 193(3):168–176

    Article  PubMed  PubMed Central  Google Scholar 

  • Konen CS, Kastner S (2008) Two hierarchically organized neural systems for object information in human visual cortex. Nat Neurosci 11(2):224–231

    Article  CAS  PubMed  Google Scholar 

  • Kourtzi Z, Kanwisher N (2001) Representation of perceived object shape by the human lateral occipital complex. Science 293(5534):1506–1509

    Article  CAS  PubMed  Google Scholar 

  • Kveraga K, Boshyan J, Bar M (2007) Magnocellular projections as the trigger of top-down facilitation in recognition. J Neurosci 27(48):13232–13240

    Article  CAS  PubMed  Google Scholar 

  • Kveraga K, Ghuman AS, Kassam KS, Aminoff EA, Hamalainen MS, Chaumon M, Bar M (2011) Early onset of neural synchronization in the contextual associations network. Proc Natl Acad Sci USA 108(8):3389–3394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamme VAF, Roelfsema PR (2000) The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci 23:571–579

    Article  CAS  PubMed  Google Scholar 

  • Larsson J, Amunts K, Gulyas B, Malikovic A, Zilles K, Roland PE (1999) Neuronal correlates of real and illusory contour perception: functional anatomy with PET. Eur J Neurosci 11(11):4024–4036

    Article  CAS  PubMed  Google Scholar 

  • Lavidor M, Walsh V (2003) A magnetic stimulation examination of orthographic neighborhood effects in visual word recognition. J Cogn Neurosci 15(3):354–363

    Article  PubMed  Google Scholar 

  • Lerner Y, Hendler T, Malach R (2002) Object-completion effects in the human lateral occipital complex. Cereb Cortex 12(2):163–177

    Article  CAS  PubMed  Google Scholar 

  • Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RB (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA 92(18):8135–8139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez A, Hillyard SA, Dias EC, Hagler DJ Jr, Butler PD, Guilfoyle DN, Jalbrzikowski M, Silipo G, Javitt DC (2008) Magnocellular pathway impairment in schizophrenia: evidence from functional magnetic resonance imaging. J Neurosci 28(30):7492–7500

    Article  CAS  PubMed  Google Scholar 

  • Martinez A, Hillyard SA, Bickel S, Dias EC, Butler PD, Javitt DC (2011) Consequences of magnocellular dysfunction on processing attended information in schizophrenia. Cereb Cortex 22:1282–1293

    Article  PubMed  Google Scholar 

  • McClintock SM, Freitas C, Oberman L, Lisanby SH, Pascual-Leone A (2011) Transcranial magnetic stimulation: a neuroscientific probe of cortical function in schizophrenia. Biol Psychiatry 70(1):19–27

    Article  PubMed  PubMed Central  Google Scholar 

  • Mendola JD, Dale AM, Fischl B, Liu AK, Tootell RB (1999) The representation of illusory and real contours in human cortical visual areas revealed by functional magnetic resonance imaging. J Neurosci 19(19):8560–8572

    CAS  PubMed  Google Scholar 

  • Murray MM, Wylie GR, Higgins BA, Javitt DC, Schroeder CE, Foxe JJ (2002) The spatiotemporal dynamics of illusory contour processing: combined high-density electrical mapping, source analysis, and functional magnetic resonance imaging. J Neurosci 22(12):5055–5073

    CAS  PubMed  Google Scholar 

  • Murray MM, Foxe DM, Javitt DC, Foxe JJ (2004) Setting boundaries: brain dynamics of modal and amodal illusory shape completion in humans. J Neurosci 24(31):6898–6903

    Article  CAS  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    Article  CAS  PubMed  Google Scholar 

  • O’Shea J, Walsh V (2006) Cognitive neuroscience: trickle-down theories of vision. Curr Biol 16(6):R206–R209

    Article  PubMed  Google Scholar 

  • Sack AT, Cohen Kadosh R, Schuhmann T, Moerel M, Walsh V, Goebel R (2009) Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J Cogn Neurosci 21(2):207–221

    Article  PubMed  Google Scholar 

  • Salvador R, Miranda PC, Roth Y, Zangen A (2009) High permeability cores to optimize the stimulation of deeply located brain regions using transcranial magnetic stimulation. Phys Med Biol 54(10):3113–3128

    Article  CAS  PubMed  Google Scholar 

  • Sehatpour P, Molholm S, Javitt DC, Foxe JJ (2006) Spatiotemporal dynamics of human object recognition processing: an integrated high-density electrical mapping and functional imaging study of “closure” processes. Neuroimage 29(2):605–618

    Article  PubMed  Google Scholar 

  • Sehatpour P, Molholm S, Schwartz TH, Mahoney JR, Mehta AD, Javitt DC, Stanton PK, Foxe JJ (2008) A human intracranial study of long-range oscillatory coherence across a frontal–occipital–hippocampal brain network during visual object processing. Proc Natl Acad Sci USA 105(11):4399–4404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sehatpour P, Dias EC, Butler PD, Revheim N, Guilfoyle DN, Foxe JJ, Javitt DC (2010) Impaired visual object processing across an occipital–frontal–hippocampal brain network in schizophrenia: an integrated neuroimaging study. Arch Gen Psychiatry 67(8):772–782

    Article  PubMed  PubMed Central  Google Scholar 

  • Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59(Suppl 20):22–33

    PubMed  Google Scholar 

  • Silvanto J, Lavie N, Walsh V (2005) Double dissociation of V1 and V5/MT activity in visual awareness. Cereb Cortex 15(11):1736–1741

    Article  PubMed  Google Scholar 

  • Snodgrass JG, Corwin J (1988) Perceptual identification thresholds for 150 fragmented pictures from the Snodgrass and Vanderwart picture set. Percept Mot Skills 67(1):3–36

    Article  CAS  PubMed  Google Scholar 

  • Straube S, Fahle M (2011) Visual detection and identification are not the same: evidence from psychophysics and fMRI. Brain Cogn 75(1):29–38

    Article  PubMed  Google Scholar 

  • Thielscher A, Kammer T (2004) Electric field properties of two commercial figure-8 coils in TMS: calculation of focality and efficiency. Clin Neurophysiol 115(7):1697–1708

    Article  PubMed  Google Scholar 

  • Vaccarino V, Kasl SV, Abramson J, Krumholz HM (2001) Depressive symptoms and risk of functional decline and death in patients with heart failure. J Am Coll Cardiol 38(1):199–205

    Article  CAS  PubMed  Google Scholar 

  • Wokke ME, Vandenbroucke AR, Scholte HS, Lamme VA (2013) Confuse your illusion: feedback to early visual cortex contributes to perceptual completion. Psychol Sci 24(1):63–71

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported in part by a research grant from the Israel Science Foundation No. 474/06, and a NARSAD Independent Investigator Grant to ML, and US Public Health Service (USPHS) Grants R37 MH49334 and P50 MH086385 to DCJ.

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Authors and Affiliations

  1. Department of Psychiatry, The Chaim Sheba Medical Center, TAU, 52621, Tel Hashomer, Israel

    Revital Amiaz, Ari A. Gershon & Mark Weiser

  2. Department of Psychology, The Gonda Multidisciplinary Brain Research Center, Bar Ilan University, 52900, Ramat Gan, Israel

    Dana Vainiger & Michal Lavidor

  3. Department of Psychology, University of Hull, Hull, UK

    Michal Lavidor

  4. Schizophrenia Research Center, Nathan Kline Institute for Psychiatric Research, Orangeburg, NY, USA

    Daniel C. Javitt

  5. Departments of Psychiatry and Neuroscience, Columbia University College of Physicians and Surgeons, New York, NY, USA

    Daniel C. Javitt

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  1. Revital Amiaz
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  2. Dana Vainiger
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  3. Ari A. Gershon
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  4. Mark Weiser
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  5. Michal Lavidor
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  6. Daniel C. Javitt
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Correspondence to Revital Amiaz.

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Amiaz, R., Vainiger, D., Gershon, A.A. et al. Applying Transcranial Magnetic Stimulation (TMS) Over the Dorsal Visual Pathway Induces Schizophrenia-like Disruption of Perceptual Closure. Brain Topogr 29, 552–560 (2016). https://doi.org/10.1007/s10548-016-0487-1

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  • DOI: https://doi.org/10.1007/s10548-016-0487-1

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