Unconscious Priming Requires Early Visual Cortex at Specific Temporal Phases of Processing

Although examples of unconscious shape priming have been well documented, whether such priming requires early visual cortex (V1/V2) has not been established. In the current study, we used TMS of V1/V2 at varying temporal intervals to suppress the visibility of preceding shape primes while the interval between primes and targets was kept constant. Our results show that, although conscious perception requires V1/V2, unconscious priming can occur without V1/V2 at an intermediate temporal interval but not at early (5–25 msec) or later (65–125 msec) stages of processing. Because the later time window of unconscious priming suppression has been proposed to interfere with feedback processing, our results further suggest that feedback processing is also essential for unconscious priming and may not be a sufficient condition for conscious vision.

[1]  Bruno G. Breitmeyer,et al.  Visual masking , 2007, Scholarpedia.

[2]  R. K. Simpson.  Nature Neuroscience , 2022 .

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

[4]  S. Geisser,et al.  On methods in the analysis of profile data , 1959 .

[5]  W Paulus,et al.  Differential inhibition of chromatic and achromatic perception by transcranial magnetic stimulation of the human visual cortex. , 1999, Neuroreport.

[6]  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.

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

[8]  Alexander T. Sack,et al.  The chronometry of visual perception: Review of occipital TMS masking studies , 2014, Neuroscience & Biobehavioral Reviews.

[9]  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.

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

[11]  N. Logothetis,et al.  Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry , 1996, Nature.

[12]  R. Held,et al.  Residual Visual Function after Brain Wounds involving the Central Visual Pathways in Man , 1973, Nature.

[13]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[14]  Ichiro Kanazawa,et al.  Shortening of simple reaction time by peripheral electrical and submotor-threshold magnetic cortical stimulation , 1997, Experimental Brain Research.

[15]  L Weiskrantz,et al.  Visual capacity in the hemianopic field following a restricted occipital ablation. , 1974, Brain : a journal of neurology.

[16]  Linda Henriksson,et al.  Unconscious response priming by shape depends on geniculostriate visual projection , 2012, The European journal of neuroscience.

[17]  Michael H. Herzog,et al.  Combining backward masking and transcranial magnetic stimulation in human observers , 2003, Neuroscience Letters.

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

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

[20]  Heiko Neumann,et al.  Ventral extra-striate cortical areas are required for human visual texture segmentation. , 2009, Journal of vision.

[21]  M. Eimer,et al.  Effects of masked stimuli on motor activation: behavioral and electrophysiological evidence. , 1998, Journal of experimental psychology. Human perception and performance.

[22]  S. Engel,et al.  Interocular rivalry revealed in the human cortical blind-spot representation , 2001, Nature.

[23]  David A. Leopold,et al.  Blindsight depends on the lateral geniculate nucleus , 2010, Nature.

[24]  Anna C Nobre,et al.  FEF TMS affects visual cortical activity. , 2006, Cerebral cortex.

[25]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[26]  D. Heeger,et al.  Activity in primary visual cortex predicts performance in a visual detection task , 2000, Nature Neuroscience.

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

[28]  Lawrence C. Sincich,et al.  Bypassing V1: a direct geniculate input to area MT , 2004, Nature Neuroscience.

[29]  M. Tamietto,et al.  Neural bases of the non-conscious perception of emotional signals , 2010, Nature Reviews Neuroscience.

[30]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

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

[32]  Tony Ro,et al.  Feedback Contributions to Visual Awareness in Human Occipital Cortex , 2003, Current Biology.

[33]  Franck Vidal,et al.  A transcranial magnetic stimulation study of information processing in the motor cortex: relationship between the silent period and the reaction time delay. , 2002, Psychophysiology.

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

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

[36]  G. Holmes.  DISTURBANCES OF VISUAL ORIENTATION , 1918, The British journal of ophthalmology.

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

[38]  M Seyal,et al.  Suppression of cutaneous perception by magnetic pulse stimulation of the human brain. , 1992, Electroencephalography and clinical neurophysiology.

[39]  Victor A. F. Lamme,et al.  Altered figure-ground perception in monkeys with an extra-striate lesion , 2007, Neuropsychologia.

[40]  Thomas Schmidt,et al.  Primes and targets in rapid chases: tracing sequential waves of motor activation. , 2006, Behavioral neuroscience.

[41]  Y. Hochberg.  A sharper Bonferroni procedure for multiple tests of significance , 1988 .

[42]  M. Yukie,et al.  Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys , 1981, The Journal of comparative neurology.

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

[44]  N K Humphrey,et al.  Vision in a Monkey without Striate Cortex: A Case Study , 1974, Perception.

[45]  Giulio Tononi,et al.  Integrated Information in Discrete Dynamical Systems: Motivation and Theoretical Framework , 2008, PLoS Comput. Biol..

[46]  J. Enns,et al.  Object Substitution: A New Form of Masking in Unattended Visual Locations , 1997 .

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

[48]  Ronald A. Rensink,et al.  Competition for consciousness among visual events: the psychophysics of reentrant visual processes. , 2000, Journal of experimental psychology. General.

[49]  J. Driver,et al.  Preparatory states in crossmodal spatial attention: spatial specificity and possible control mechanisms , 2003, Experimental Brain Research.

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

[51]  V. Lamme,et al.  Repression of unconscious information by conscious processing: evidence from affective blindsight induced by transcranial magnetic stimulation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[52]  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.

[53]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[54]  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.

[55]  R S Nickerson,et al.  Intersensory facilitation of reaction time: energy summation or preparation enhancement? , 1973, Psychological review.

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

[57]  P Girard,et al.  Feedback connections act on the early part of the responses in monkey visual cortex. , 2001, Journal of neurophysiology.

[58]  Jonathan D. Cohen,et al.  Reproducibility Distinguishes Conscious from Nonconscious Neural Representations , 2010, Science.

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

[60]  M. Gazzaniga,et al.  Residual vision in a scotoma: implications for blindsight. , 1992, Science.

[61]  L. Weiskrantz.  Blindsight : a case study and implications , 1986 .

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

[63]  M. Goodale,et al.  The visual brain in action , 1995 .

[64]  C. Gilbert,et al.  Brain States: Top-Down Influences in Sensory Processing , 2007, Neuron.

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

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

[67]  K. Yu,et al.  Attentional modulation of sensorimotor processes in the absence of perceptual awareness , 2006, Proceedings of the National Academy of Sciences.

[68]  A Cohen,et al.  Extrageniculate vision in hemianopic humans: saccade inhibition by signals in the blind field. , 1990, Science.

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

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

[71]  Tony Ro,et al.  Unconscious Color Priming Occurs at Stimulus- Not Percept-Dependent Levels of Processing , 2004, Psychological science.

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

[73]  L Weiskrantz,et al.  Residual vision in a scotoma. A follow-up study of 'form' discrimination. , 1987, Brain : a journal of neurology.

[74]  D. Heeger,et al.  Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry , 2000, Nature Neuroscience.

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

[76]  Victor A. F. Lamme,et al.  Zap! Magnetic tricks on conscious and unconscious vision , 2006, Trends in Cognitive Sciences.

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

[78]  W. Fries.  The projection from the lateral geniculate nucleus to the prestriate cortex of the macaque monkey , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[79]  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.

[80]  J. Silvanto,et al.  Distinct Causal Mechanisms of Attentional Guidance by Working Memory and Repetition Priming in Early Visual Cortex , 2012, The Journal of Neuroscience.

[81]  S. Martinez-Conde,et al.  The role of feedback in visual masking and visual processing , 2008, Advances in cognitive psychology.

[82]  D. Mumford,et al.  Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency , 2002, Nature Neuroscience.

[83]  Philippe Kahane,et al.  Neural repetition suppression in ventral occipito-temporal cortex occurs during conscious and unconscious processing of frequent stimuli , 2014, NeuroImage.