The role of awareness in shaping responses in human visual cortex

The visual cortex contains information about stimuli even when they are not consciously perceived. However, it remains unknown whether the visual system integrates local features into global objects without awareness. Here, we tested this by measuring brain activity in human observers viewing fragmented shapes that were either visible or rendered invisible by fast counterphase flicker. We then projected measured neural responses to these stimuli back into visual space. Visible stimuli caused robust responses reflecting the positions of their component fragments. Their neural representations also strongly resembled one another regardless of local features. By contrast, representations of invisible stimuli differed from one another and, crucially, also from visible stimuli. Our results demonstrate that even the early visual cortex encodes unconscious visual information differently from conscious information, presumably by only encoding local features. This could explain previous conflicting behavioural findings on unconscious visual processing.

[1]  L. Deouell,et al.  Neuroscientific Evidence for Processing Without Awareness. , 2022, Annual review of neuroscience.

[2]  M. Sereno,et al.  Topological Maps and Brain Computations From Low to High , 2022, Frontiers in Systems Neuroscience.

[3]  D. S. Schwarzkopf,et al.  The human primary visual cortex (V1) encodes the perceived position of static but not moving objects , 2021, Communications Biology.

[4]  P. Winklewski,et al.  Critical Flicker Fusion Frequency: A Narrative Review , 2021, Medicina.

[5]  Roberto Santana,et al.  Informative neural representations of unseen contents during higher-order processing in human brains and deep artificial networks , 2021, Nature Human Behaviour.

[6]  Nonie Finlayson,et al.  Topographic signatures of global object perception in human visual cortex , 2019, NeuroImage.

[7]  J. Dubois,et al.  Imaging object-scene relations processing in visible and invisible natural scenes , 2019, Scientific Reports.

[8]  Ying Wang,et al.  Subconscious processing reveals dissociable contextual modulations of visual size perception , 2018, Cognition.

[9]  Rainer Goebel,et al.  Reconstructing imagined letters from early visual cortex reveals tight topographic correspondence between visual mental imagery and perception , 2018, Brain Structure and Function.

[10]  Y. Sugita,et al.  Size-contrast illusion induced by unconscious context. , 2018, Journal of vision.

[11]  L. Mudrik,et al.  Evidence for Implicit—But Not Unconscious—Processing of Object-Scene Relations , 2018, Psychological science.

[12]  P. R. Montoro,et al.  Global shape integration and illusory form perception in the absence of awareness , 2017, Consciousness and Cognition.

[13]  Johannes Jacobus Fahrenfort,et al.  Perceptual integration without conscious access , 2016, Proceedings of the National Academy of Sciences.

[14]  Johan Wagemans,et al.  Scene Integration Without Awareness , 2016, Psychological science.

[15]  D. Schwarzkopf,et al.  Induction of Kanizsa Contours Requires Awareness of the Inducing Context , 2016, bioRxiv.

[16]  J. Wagemans,et al.  No evidence for surface organization in Kanizsa configurations during continuous flash suppression , 2015, Attention, Perception, & Psychophysics.

[17]  Stanislas Dehaene,et al.  Cortical activity is more stable when sensory stimuli are consciously perceived , 2015, Proceedings of the National Academy of Sciences.

[18]  F. D. Lange,et al.  Shape Perception Simultaneously Up- and Downregulates Neural Activity in the Primary Visual Cortex , 2014, Current Biology.

[19]  Johannes Jacobus Fahrenfort,et al.  Seeing without Knowing: Neural Signatures of Perceptual Inference in the Absence of Report , 2014, Journal of Cognitive Neuroscience.

[20]  C. Koch,et al.  Differential processing of invisible congruent and incongruent scenes: a case for unconscious integration. , 2013, Journal of vision.

[21]  Victor A. F. Lamme,et al.  Confuse Your Illusion , 2013, Psychological science.

[22]  Xuchu Weng,et al.  Perceptual Grouping without Awareness: Superiority of Kanizsa Triangle in Breaking Interocular Suppression , 2012, PloS one.

[23]  Jonas Larsson,et al.  fMRI repetition suppression: neuronal adaptation or stimulus expectation? , 2012, Cerebral cortex.

[24]  P. Sterzer,et al.  Breaking Continuous Flash Suppression: A New Measure of Unconscious Processing during Interocular Suppression? , 2011, Front. Hum. Neurosci..

[25]  Dominique Lamy,et al.  Integration without awareness: expanding the limits of unconscious processing , 2011 .

[26]  Dominique Lamy,et al.  Integration Without Awareness , 2011, Psychological science.

[27]  D. Schwarzkopf,et al.  Contextual Illusions Reveal the Limit of Unconscious Visual Processing , 2011, Psychological science.

[28]  D. Samuel Schwarzkopf,et al.  Interpreting local visual features as a global shape requires awareness , 2010, Proceedings of the Royal Society B: Biological Sciences.

[29]  Huafu Chen,et al.  Neural mechanism of unconscious perception of surprised facial expression , 2010, NeuroImage.

[30]  D. Macleod,et al.  Imperceptibly rapid contrast modulations processed in cortex: Evidence from psychophysics. , 2010, Journal of Vision.

[31]  B. Wandell,et al.  Mapping Hv4 and Ventral Occipital Cortex: the Venous Eclipse , 2022 .

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

[33]  R. Blake,et al.  Suppression During Binocular Rivalry Broadens Orientation Tuning , 2009, Psychological science.

[34]  G. Rees,et al.  Fine-scale activity patterns in high-level visual areas encode the category of invisible objects. , 2008, Journal of vision.

[35]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.

[36]  Edward Vul,et al.  Contingent aftereffects distinguish conscious and preconscious color processing , 2006, Nature Neuroscience.

[37]  C. Koch,et al.  Continuous flash suppression reduces negative afterimages , 2005, Nature Neuroscience.

[38]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

[39]  Justin A. Harris,et al.  Contextual Modulation outside of Awareness , 2005, Current Biology.

[40]  Patrik Vuilleumier,et al.  Effects of Low-Spatial Frequency Components of Fearful Faces on Fusiform Cortex Activity , 2003, Current Biology.

[41]  N. Logothetis The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal , 2003, The Journal of Neuroscience.

[42]  S Zeki,et al.  The relationship between cortical activation and perception investigated with invisible stimuli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[44]  Sheng He,et al.  Orientation-selective adaptation and tilt after-effect from invisible patterns , 2001, Nature.

[45]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

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

[48]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[49]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  Edward H. Adelson,et al.  The delayed rod afterimage , 1982, Vision Research.

[51]  C. Spearman CORRELATION CALCULATED FROM FAULTY DATA , 1910 .

[52]  C. Koch,et al.  Low-level awareness accompanies "unconscious" high-level processing during continuous flash suppression. , 2016, Journal of vision.

[53]  Omar H. Butt,et al.  The retinotopic organization of striate cortex is well predicted by surface topology Supplemental Information , 2012 .