The threshold for conscious report: Signal loss and response bias in visual and frontal cortex

Setting conscious perception alight What are the neuronal mechanisms that enable conscious perception? Why do some images remain subliminal? Van Vugt et al. trained monkeys to detect low-contrast images and compared neuronal activity in brain areas V1, V4, and the dorsolateral prefrontal cortex. Some stimuli made it into consciousness, and others were subliminal depending on their propagation, which can be variable for weak stimuli (see the Perspective by Mashour). Strongly propagated stimuli initiated a state in the higher brain areas called “ignition” that caused information about a brief stimulus to become sustained and broadcasted back through recurrent interactions between many brain areas. Science, this issue p. 537; see also p. 493 Weak stimuli reach conscious perception only if they are propagated well enough to cross a threshold in higher cortical areas. Why are some visual stimuli consciously detected, whereas others remain subliminal? We investigated the fate of weak visual stimuli in the visual and frontal cortex of awake monkeys trained to report stimulus presence. Reported stimuli were associated with strong sustained activity in the frontal cortex, and frontal activity was weaker and quickly decayed for unreported stimuli. Information about weak stimuli could be lost at successive stages en route from the visual to the frontal cortex, and these propagation failures were confirmed through microstimulation of area V1. Fluctuations in response bias and sensitivity during perception of identical stimuli were traced back to prestimulus brain-state markers. A model in which stimuli become consciously reportable when they elicit a nonlinear ignition process in higher cortical areas explained our results.

[1]  E. J. Tehovnik,et al.  Saccadic eye movements evoked by microstimulation of striate cortex , 2003, The European journal of neuroscience.

[2]  C. Kufta,et al.  Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex. , 1996, Brain : a journal of neurology.

[3]  P. Roelfsema,et al.  Chronic multiunit recordings in behaving animals: advantages and limitations. , 2005, Progress in brain research.

[4]  Simon Hanslmayr,et al.  Prestimulus oscillations predict visual perception performance between and within subjects , 2007, NeuroImage.

[5]  W. Einhäuser,et al.  Binocular Rivalry: Frontal Activity Relates to Introspection and Action But Not to Perception , 2014, The Journal of Neuroscience.

[6]  Christopher J. Aura,et al.  Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey , 2008, Nature Neuroscience.

[7]  E. Seidemann,et al.  Linking Neuronal and Behavioral Performance in a Reaction-Time Visual Detection Task , 2007, The Journal of Neuroscience.

[8]  J. Schoffelen,et al.  Prestimulus Oscillatory Activity in the Alpha Band Predicts Visual Discrimination Ability , 2008, The Journal of Neuroscience.

[9]  Xiao-Jing Wang,et al.  A diversity of localized timescales in network activity , 2014, eLife.

[10]  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 .

[11]  Sharif I. Kronemer,et al.  A Switch and Wave of Neuronal Activity in the Cerebral Cortex During the First Second of Conscious Perception , 2019, Cerebral cortex.

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

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

[14]  J. Changeux,et al.  Ongoing Spontaneous Activity Controls Access to Consciousness: A Neuronal Model for Inattentional Blindness , 2005, PLoS biology.

[15]  C. Tallon-Baudry,et al.  How Ongoing Fluctuations in Human Visual Cortex Predict Perceptual Awareness: Baseline Shift versus Decision Bias , 2009, The Journal of Neuroscience.

[16]  R. Quiroga,et al.  Human single-neuron responses at the threshold of conscious recognition , 2008, Proceedings of the National Academy of Sciences.

[17]  Michael J. Goard,et al.  Fast Modulation of Visual Perception by Basal Forebrain Cholinergic Neurons , 2013, Nature Neuroscience.

[18]  A. Seth.  Consciousness: The last 50 years (and the next) , 2018, Brain and neuroscience advances.

[19]  C. Koch,et al.  Neural correlates of consciousness: progress and problems , 2016, Nature Reviews Neuroscience.

[20]  Sébastien M. Crouzet,et al.  Spontaneous Neural Oscillations Bias Perception by Modulating Baseline Excitability , 2017, The Journal of Neuroscience.

[21]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[22]  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.

[23]  Stephen V. David,et al.  Cortical Membrane Potential Signature of Optimal States for Sensory Signal Detection , 2015, Neuron.

[24]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[25]  B. Baars.  The conscious access hypothesis: origins and recent evidence , 2002, Trends in Cognitive Sciences.

[26]  Houman Safaai,et al.  Coordinated Population Activity Underlying Texture Discrimination in Rat Barrel Cortex , 2013, The Journal of Neuroscience.

[27]  UnCheol Lee,et al.  Disruption of Frontal–Parietal Communication by Ketamine, Propofol, and Sevoflurane , 2013, Anesthesiology.

[28]  P. Rossini,et al.  Pre- and poststimulus alpha rhythms are related to conscious visual perception: a high-resolution EEG study. , 2005, Cerebral cortex.

[29]  S Dehaene,et al.  A model of subjective report and objective discrimination as categorical decisions in a vast representational space , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[30]  P. Roelfsema,et al.  Simultaneous selection by object-based attention in visual and frontal cortex , 2014, Proceedings of the National Academy of Sciences.

[31]  I. Fried,et al.  Neural “Ignition”: Enhanced Activation Linked to Perceptual Awareness in Human Ventral Stream Visual Cortex , 2009, Neuron.

[32]  George H. Denfield,et al.  Pupil Fluctuations Track Fast Switching of Cortical States during Quiet Wakefulness , 2014, Neuron.

[33]  T. Ergenoğlu,et al.  Alpha rhythm of the EEG modulates visual detection performance in humans. , 2004, Brain research. Cognitive brain research.

[34]  Gustavo Deco,et al.  Neuronal Discharges and Gamma Oscillations Explicitly Reflect Visual Consciousness in the Lateral Prefrontal Cortex , 2012, Neuron.

[35]  R. Romo,et al.  Neuronal correlates of subjective sensory experience , 2005, Nature Neuroscience.

[36]  V. Lamme,et al.  No-Report Paradigms: Extracting the True Neural Correlates of Consciousness , 2015, Trends in Cognitive Sciences.

[37]  Joshua J. LaRocque,et al.  The neural correlates of dreaming , 2014, Nature Neuroscience.

[38]  Xiao-Jing Wang.  Decision Making in Recurrent Neuronal Circuits , 2008, Neuron.

[39]  Anthony G. Hudetz,et al.  Differential Role of Prefrontal and Parietal Cortices in Controlling Level of Consciousness , 2018, Current Biology.

[40]  F. Wendling,et al.  COALIA: A Computational Model of Human EEG for Consciousness Research , 2019, Frontiers in systems neuroscience.

[41]  Jan Theeuwes,et al.  The Role of Awareness in Processing of Oculomotor Capture: Evidence from Event-related Potentials , 2008, Journal of Cognitive Neuroscience.

[42]  Michelle J. Redinbaugh,et al.  Thalamus Modulates Consciousness via Layer-Specific Control of Cortex , 2020, Neuron.

[43]  R. Shapley,et al.  Spatial Spread of the Local Field Potential and its Laminar Variation in Visual Cortex , 2009, The Journal of Neuroscience.

[44]  J. Changeux,et al.  Experimental and Theoretical Approaches to Conscious Processing , 2011, Neuron.

[45]  Michael X Cohen,et al.  Analyzing Neural Time Series Data: Theory and Practice , 2014 .

[46]  G. Tononi,et al.  Consciousness and Anesthesia , 2008, Science.

[47]  T. Hendler,et al.  Contrast sensitivity in human visual areas and its relationship to object recognition. , 2002, Journal of neurophysiology.

[48]  H. Lau,et al.  A detection theoretic explanation of blindsight suggests a link between conscious perception and metacognition , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[49]  P. Roelfsema,et al.  Distinct Feedforward and Feedback Effects of Microstimulation in Visual Cortex Reveal Neural Mechanisms of Texture Segregation , 2017, Neuron.

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

[51]  A. Villringer,et al.  Heart–brain interactions shape somatosensory perception and evoked potentials , 2019, Proceedings of the National Academy of Sciences.

[52]  K. Linkenkaer-Hansen,et al.  Prestimulus Oscillations Enhance Psychophysical Performance in Humans , 2004, The Journal of Neuroscience.