The spatiotemporal profile of cortical processing leading up to visual perception.

Much controversy exists around the locus of conscious visual perception in human cortex. Some authors have proposed that its neural correlates correspond with recurrent processing within visual cortex, whereas others have argued they are located in a frontoparietal network. The present experiment aims to bring together these competing viewpoints. We recorded EEG from human subjects that were engaged in detecting masked visual targets. From this, we obtained a spatiotemporal profile of neural activity selectively related to the processing of the targets, which we correlated with the subjects' ability to detect those targets. This made it possible to distinguish between those stages of visual processing that correlate with human perception and those that do not. The results show that target induced extra-striate feedforward activity peaking at 121 ms does not correlate with perception, whereas more posterior recurrent activity peaking at 160 ms does. Several subsequent stages show an alternating pattern of frontoparietal and occipital activity, all of which correlate highly with perception. This shows that perception emerges early on, but only after an initial feedforward volley, and suggests that multiple reentrant loops are involved in propagating this signal to frontoparietal areas.

[1]  S. Hillyard,et al.  Electrical Signs of Selective Attention in the Human Brain , 1973, Science.

[2]  P. Nunez,et al.  Electric fields of the brain , 1981 .

[3]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[4]  Arnulf Remole,et al.  VISUAL MASKING: AN INTEGRATIVE APPROACH , 1985 .

[5]  E. Donchin,et al.  Is the P300 component a manifestation of context updating? , 1988, Behavioral and Brain Sciences.

[6]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[7]  D. Perrett,et al.  Time course of neural responses discriminating different views of the face and head. , 1992, Journal of neurophysiology.

[8]  Victor A. F. Lamme,et al.  Texture segregation is processed by primary visual cortex in man and monkey. Evidence from VEP experiments , 1992, Vision Research.

[9]  Henk Spekreijse,et al.  Contour from motion processing occurs in primary visual cortex , 1993, Nature.

[10]  Victor A. F. Lamme The neurophysiology of figure-ground segregation in primary visual cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[12]  Denis Fize,et al.  Speed of processing in the human visual system , 1996, Nature.

[13]  S. Luck,et al.  Bridging the Gap between Monkey Neurophysiology and Human Perception: An Ambiguity Resolution Theory of Visual Selective Attention , 1997, Cognitive Psychology.

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

[15]  Victor A. F. Lamme,et al.  Figure-ground activity in primary visual cortex is suppressed by anesthesia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[17]  Clara Casco,et al.  A visual evoked potential correlate of global figure-ground segmentation , 1999, Vision Research.

[18]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[19]  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.

[20]  Victor A. F. Lamme,et al.  Separate processing dynamics for texture elements, boundaries and surfaces in primary visual cortex of the macaque monkey. , 1999, Cerebral cortex.

[21]  M. Mesulam Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[23]  B. Breitmeyer,et al.  Recent models and findings in visual backward masking: A comparison, review, and update , 2000, Perception & psychophysics.

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

[25]  A. Kok On the utility of P3 amplitude as a measure of processing capacity. , 2001, Psychophysiology.

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

[27]  T. Wickens Elementary Signal Detection Theory , 2001 .

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

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

[30]  H. Spekreijse,et al.  FigureGround Segregation in a Recurrent Network Architecture , 2002, Journal of Cognitive Neuroscience.

[31]  N. Kanwisher,et al.  Stages of processing in face perception: an MEG study , 2002, Nature Neuroscience.

[32]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[33]  H. Spekreijse,et al.  Masking Interrupts Figure-Ground Signals in V1 , 2002, Journal of Cognitive Neuroscience.

[34]  Delphine Pins,et al.  The neural correlates of conscious vision. , 2003, Cerebral cortex.

[35]  Victor A. F. Lamme,et al.  Source (or Part of the following Source): Type Article Title Internal State of Monkey Primary Visual Cortex (v1) Predicts Figure Ground Perception Author(s) Internal State of Monkey Primary Visual Cortex (v1) Predicts Figure–ground Perception Materials and Methods , 2022 .

[36]  C. Koch,et al.  Visual Selective Behavior Can Be Triggered by a Feed-Forward Process , 2003, Journal of Cognitive Neuroscience.

[37]  J. Changeux,et al.  A neuronal network model linking subjective reports and objective physiological data during conscious perception , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[38]  G. Woodman,et al.  Dissociations Among Attention, Perception, and Awareness During Object-Substitution Masking , 2003, Psychological science.

[39]  V. Lamme Why visual attention and awareness are different , 2003, Trends in Cognitive Sciences.

[40]  A. Engel,et al.  Event-related potential correlates of the attentional blink phenomenon. , 2003, Brain research. Cognitive brain research.

[41]  P. Schyns,et al.  Receptive Fields for Flexible Face Categorizations , 2004, Psychological science.

[42]  Antti Revonsuo,et al.  An electrophysiological correlate of human visual awareness , 2004, Neuroscience Letters.

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

[44]  J. Driver,et al.  Visibility Reflects Dynamic Changes of Effective Connectivity between V1 and Fusiform Cortex , 2005, Neuron.

[45]  S. Dehaene,et al.  Timing of the brain events underlying access to consciousness during the attentional blink , 2005, Nature Neuroscience.

[46]  M. Koivisto,et al.  Independence of visual awareness from attention at early processing stages , 2005, Neuroreport.

[47]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

[48]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Victor A. F. Lamme,et al.  The influence of inattention on the neural correlates of scene segmentation , 2006, Brain Research.

[50]  R. Ratcliff,et al.  Neural Representation of Task Difficulty and Decision Making during Perceptual Categorization: A Timing Diagram , 2006, The Journal of Neuroscience.

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

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

[53]  D. Kersten,et al.  The representation of perceived angular size in human primary visual cortex , 2006, Nature Neuroscience.

[54]  Minna Lehtonen,et al.  Independence of visual awareness from the scope of attention: an electrophysiological study. , 2006, Cerebral cortex.

[55]  P. Sajda,et al.  Temporal characterization of the neural correlates of perceptual decision making in the human brain. , 2006, Cerebral cortex.

[56]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[57]  Johannes J. Fahrenfort,et al.  Masking Disrupts Reentrant Processing in Human Visual Cortex , 2007, Journal of Cognitive Neuroscience.