Transcranial Magnetic Stimulation of the Human Frontal Eye ®eld Facilitates Visual Awareness

What are the brain mechanisms allowing a stimulus to enter our awareness? Some theories suggest that this process engages resources overlapping with those required for action control, but experimental support for these ideas is still required. Here, we investigated whether the human frontal eye field (FEF), an area known to control eye movements, is involved in visual awareness. Volunteers participated in a backward masking task in which they were able to detect a target in a small proportion of trials. We observed that a single pulse of transcranial magnetic stimulation applied over the FEF shortly before the target's onset facilitated visual sensitivity; subjects were able to detect an otherwise subliminal object. These results show that modulating the neuronal activity of the FEF can enhance visual detection, thereby yielding new insights into the neural basis of visual awareness.

[1]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[2]  A. Vighetto,et al.  A selective imaging of tinnitus. , 1999, Neuroreport.

[3]  L Weiskrantz,et al.  Pattern of neuronal activity associated with conscious and unconscious processing of visual signals. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Enns,et al.  What’s new in visual masking? , 2000, Trends in Cognitive Sciences.

[5]  G. Thickbroom,et al.  Transcranial magnetic stimulation of the human frontal eye field , 1996, Journal of the Neurological Sciences.

[6]  R H Carpenter,et al.  Visual selection: Neurons that make up their minds , 1999, Current Biology.

[7]  H. Kennedy,et al.  Laminar Distribution of Neurons in Extrastriate Areas Projecting to Visual Areas V1 and V4 Correlates with the Hierarchical Rank and Indicates the Operation of a Distance Rule , 2000, The Journal of Neuroscience.

[8]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[9]  M. Hallett,et al.  Human motor evoked responses to paired transcranial magnetic stimuli. , 1992, Electroencephalography and clinical neurophysiology.

[10]  C. Koch,et al.  Consciousness and neuroscience. , 1998, Cerebral cortex.

[11]  G. Mangun,et al.  Covariations in ERP and PET measures of spatial selective attention in human extrastriate visual cortex , 1997, Human brain mapping.

[12]  C M Michel,et al.  Visual activity in the human frontal eye field. , 1999, Neuroreport.

[13]  T. Paus,et al.  Transcranial Magnetic Stimulation of the Human Frontal Eye Field: Effects on Visual Perception and Attention , 2002, Journal of Cognitive Neuroscience.

[14]  J. Schall,et al.  Antecedents and correlates of visual detection and awareness in macaque prefrontal cortex , 2000, Vision Research.

[15]  T. Paus.  Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[16]  J. Gold,et al.  Neural computations that underlie decisions about sensory stimuli , 2001, Trends in Cognitive Sciences.

[17]  Á. Pascual-Leone,et al.  Modulation of intracortical neuronal circuits in human hand motor area by digit stimulation , 2003, Experimental Brain Research.

[18]  M. Livingstone,et al.  Neuronal correlates of visibility and invisibility in the primate visual system , 1998, Nature Neuroscience.

[19]  H. Deubel,et al.  Saccade target selection and object recognition: Evidence for a common attentional mechanism , 1996, Vision Research.

[20]  A. Cowey,et al.  Visual field defects after frontal eye-field lesions in monkeys. , 1971, Brain research.

[21]  Victor A. F. Lamme.  Blindsight: the role of feedforward and feedback corticocortical connections. , 2001, Acta psychologica.

[22]  J. Schall.  Visuomotor Areas of the Frontal Lobe , 1997 .

[23]  T Moore,et al.  Control of eye movements and spatial attention. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[25]  J. Schall,et al.  Countermanding saccades in macaque , 1995, Visual Neuroscience.

[26]  Jeffrey D. Schall,et al.  The detection of visual signals by macaque frontal eye field during masking , 1999, Nature Neuroscience.

[27]  Bruno G. Breitmeyer,et al.  Visual masking : an integrative approach , 1984 .

[28]  A. Cowey,et al.  The role of the parietal cortex in visual attention—hemispheric asymmetries and the effects of learning: a magnetic stimulation study , 1998, Neuropsychologia.

[29]  C. W. Hess,et al.  Transcranial stimulation of the human frontal eye field by magnetic pulses , 2004, Experimental Brain Research.

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

[31]  R. Rafal,et al.  Neural fate of seen and unseen faces in visuospatial neglect: A combined event-related functional MRI and event-related potential study , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[33]  V. S. Ramachandran,et al.  Visual attention modulates metacontrast masking , 1995, Nature.

[34]  A. Treisman,et al.  Perceiving visually presented objets: recognition, awareness, and modularity , 1998, Current Opinion in Neurobiology.

[35]  Jeffrey D Schall,et al.  The neural selection and control of saccades by the frontal eye field. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[36]  Junying Yuan,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2022 .

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

[38]  G. Rees,et al.  Covariation of activity in visual and prefrontal cortex associated with subjective visual perception. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J B Poline,et al.  Cerebral mechanisms of word masking and unconscious repetition priming , 2001, Nature Neuroscience.

[40]  B Jouve,et al.  A mathematical approach to the connectivity between the cortical visual areas of the macaque monkey. , 1998, Cerebral cortex.

[41]  M Corbetta,et al.  Multiple neural correlates of detection in the human brain. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[42]  A. Berthoz,et al.  Neural Basis of Decision in Perception and in the Control of Movement , 1996 .