Transcranial magnetic stimulation of early visual cortex interferes with subjective visual awareness and objective forced-choice performance

In order to study whether there exist a period of activity in the human early visual cortex that contributes exclusively to visual awareness, we applied transcranial magnetic stimulation (TMS) over the early visual cortex and measured subjective visual awareness during visual forced-choice symbol or orientation discrimination tasks. TMS produced one dip in awareness 60-120 ms after stimulus onset, while forced-choice orientation discrimination was suppressed between 60 and 90 ms and symbol discrimination between 60 and 120 ms. Thus, a time window specific to visual awareness was found only in the orientation condition at 120 ms. The results imply that both conscious and unconscious perception depend on activity in early visual areas. On the basis of previous estimates of neural processing speed, we suggest that the late part of the activity period most likely involve local extrastriate-striate interactions which provide the contents for visual awareness but are not themselves sufficient for awareness to arise.

[1]  A T Barker,et al.  Transcranial magnetic stimulation. Which part of the current waveform causes the stimulation? , 2001, Experimental brain research.

[2]  H. Spekreijse,et al.  Two distinct modes of sensory processing observed in monkey primary visual cortex (V1) , 2001, Nature Neuroscience.

[3]  Rainer Goebel,et al.  Symbolic action priming relies on intact neural transmission along the retino-geniculo-striate pathway , 2009, NeuroImage.

[4]  S. Hochstein,et al.  View from the Top Hierarchies and Reverse Hierarchies in the Visual System , 2002, Neuron.

[5]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[6]  V. Amassian,et al.  Suppression of visual perception by magnetic coil stimulation of human occipital cortex. , 1989, Electroencephalography and clinical neurophysiology.

[7]  James Danckert,et al.  Blindsight in action: what can the different sub-types of blindsight tell us about the control of visually guided actions? , 2005, Neuroscience & Biobehavioral Reviews.

[8]  V. Lamme Towards a true neural stance on consciousness , 2006, Trends in Cognitive Sciences.

[9]  V. Hömberg,et al.  Impairment of visual perception and visual short term memory scanning by transcranial magnetic stimulation of occipital cortex , 2004, Experimental Brain Research.

[10]  Mika Koivisto,et al.  The relationship between awareness and attention: Evidence from ERP responses , 2009, Neuropsychologia.

[11]  A. Barker,et al.  Transcranial magnetic stimulation , 2001, Experimental Brain Research.

[12]  Mark Hallett,et al.  Two periods of processing in the (circum)striate visual cortex as revealed by transcranial magnetic stimulation , 1998, Neuropsychologia.

[13]  Juha Silvanto,et al.  The role of early visual cortex (V1/V2) in conscious and unconscious visual perception , 2010, NeuroImage.

[14]  D. Pollen Fundamental requirements for primary visual perception. , 2008, Cerebral cortex.

[15]  E. Sutter,et al.  M and P Components of the VEP and their Visual Field Distribution , 1997, Vision Research.

[16]  T L Babb,et al.  Visual receptive fields and response properties of neurons in human temporal lobe and visual pathways. , 1983, Brain : a journal of neurology.

[17]  C. N. Boehler,et al.  Rapid recurrent processing gates awareness in primary visual cortex , 2008, Proceedings of the National Academy of Sciences.

[18]  G. V. Simpson,et al.  Flow of activation from V1 to frontal cortex in humans , 2001, Experimental Brain Research.

[19]  Jens Bo Nielsen,et al.  Action-blindsight in healthy subjects after transcranial magnetic stimulation , 2008, Proceedings of the National Academy of Sciences.

[20]  David J. Heeger,et al.  Neuronal correlates of perception in early visual cortex , 2003, Nature Neuroscience.

[21]  N. Block Two neural correlates of consciousness , 2005, Trends in Cognitive Sciences.

[22]  Ryota Kanai,et al.  TMS over the intraparietal sulcus induces perceptual fading. , 2008, Journal of neurophysiology.

[23]  A Reichenbach,et al.  The cortical site of visual suppression by transcranial magnetic stimulation. , 2007, Cerebral cortex.

[24]  E Corthout,et al.  Suppression of vision by transcranial magnetic stimulation: a third mechanism , 2000, Neuroreport.

[25]  J. Sarvas Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[26]  C. Koch,et al.  Are we aware of neural activity in primary visual cortex? , 1995, Nature.

[27]  Rainer Goebel,et al.  The temporal characteristics of motion processing in hMT/V5+: Combining fMRI and neuronavigated TMS , 2006, NeuroImage.

[28]  E Corthout,et al.  Timing of activity in early visual cortex as revealed by transcranial magnetic stimulation. , 1999, Neuroreport.

[29]  J. Schwarzbach,et al.  Different time courses for visual perception and action priming , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[31]  L. Heller,et al.  Brain stimulation using electromagnetic sources: theoretical aspects. , 1992, Biophysical journal.

[32]  Tony Ro,et al.  Extrageniculate mediation of unconscious vision in transcranial magnetic stimulation-induced blindsight. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[33]  R. Hari,et al.  Coinciding early activation of the human primary visual cortex and anteromedial cuneus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[35]  J. Changeux,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 Conscious, preconscious, and subliminal processing: a testable taxonomy , 2022 .

[36]  Alvaro Pascual-Leone,et al.  Transcranial magnetic stimulation: a neurochromometrics of mind. , 2003 .

[37]  A. Cowey,et al.  Striate cortex (V1) activity gates awareness of motion , 2005, Nature Neuroscience.

[38]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[39]  Ehud Zohary,et al.  Two Phases of V1 Activity for Visual Recognition of Natural Images , 2010, Journal of Cognitive Neuroscience.

[40]  Bruno G. Breitmeyer,et al.  A comparison of masking by visual and transcranial magnetic stimulation: implications for the study of conscious and unconscious visual processing , 2004, Consciousness and Cognition.

[41]  Juha Silvanto,et al.  Double dissociation of V1 and V5/MT activity in visual awareness. , 2005, Cerebral cortex.

[42]  S. Zeki,et al.  Toward a Theory of Visual Consciousness , 1999, Consciousness and Cognition.

[43]  Linda Henriksson,et al.  Multifocal fMRI mapping of visual cortical areas , 2005, NeuroImage.

[44]  Mark Hallett,et al.  Interference with vision by TMS over the occipital pole: a fourth period , 2003, Neuroreport.

[45]  H. Masur,et al.  Suppression of visual perception by transcranial magnetic stimulation--experimental findings in healthy subjects and patients with optic neuritis. , 1993, Electroencephalography and clinical neurophysiology.

[46]  Tony Ro,et al.  Unconscious processing of orientation and color without primary visual cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Victor A. F. Lamme,et al.  Feedforward, horizontal, and feedback processing in the visual cortex , 1998, Current Opinion in Neurobiology.

[48]  Á. Pascual-Leone,et al.  Fast Backprojections from the Motion to the Primary Visual Area Necessary for Visual Awareness , 2001, Science.

[49]  T. Ro Unconscious vision in action , 2008, Neuropsychologia.

[50]  T. Kammer,et al.  Transcranial magnetic stimulation in the visual system. I. The psychophysics of visual suppression , 2004, Experimental Brain Research.

[51]  Mark Hallett,et al.  Early visual cortical processing suggested by transcranial magnetic stimulation , 2002, Neuroreport.