Neural Correlates of Subliminal Language Processing

Language is a high-level cognitive function, so exploring the neural correlates of unconscious language processing is essential for understanding the limits of unconscious processing in general. The results of several functional magnetic resonance imaging studies have suggested that unconscious lexical and semantic processing is confined to the posterior temporal lobe, without involvement of the frontal lobe—the regions that are indispensable for conscious language processing. However, previous studies employed a similarly designed masked priming paradigm with briefly presented single and contextually unrelated words. It is thus possible, that the stimulation level was insufficiently strong to be detected in the high-level frontal regions. Here, in a high-resolution fMRI and multivariate pattern analysis study we explored the neural correlates of subliminal language processing using a novel paradigm, where written meaningful sentences were suppressed from awareness for extended duration using continuous flash suppression. We found that subjectively and objectively invisible meaningful sentences and unpronounceable nonwords could be discriminated not only in the left posterior superior temporal sulcus (STS), but critically, also in the left middle frontal gyrus. We conclude that frontal lobes play a role in unconscious language processing and that activation of the frontal lobes per se might not be sufficient for achieving conscious awareness.

[1]  P. Broca Remarques sur le siège de la faculté du langage articulé, suivies d'une observation d'aphémie (perte de la parole) , 1861 .

[2]  P. Broca,et al.  Remarques sur le siege de la faculte du langage articule suivies d'une observation d'aphemie , 1861 .

[3]  W. Miles Ocular dominance in human adults. , 1930 .

[4]  A. Marcel Conscious and unconscious perception: Experiments on visual masking and word recognition , 1983, Cognitive Psychology.

[5]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[6]  K L Shapiro,et al.  Temporary suppression of visual processing in an RSVP task: an attentional blink? . , 1992, Journal of experimental psychology. Human perception and performance.

[7]  Richard S. J. Frackowiak,et al.  The role of the right hemisphere in the interpretation of figurative aspects of language. A positron emission tomography activation study. , 1994, Brain : a journal of neurology.

[8]  S Dehaene,et al.  A neuronal model of a global workspace in effortful cognitive tasks. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[9]  E. Vogel,et al.  Electrophysiological Evidence for a Postperceptual Locus of Suppression during the Attentional Blink Time-based Attention and the Attentional Blink , 1998 .

[10]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[11]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[12]  Richard L. Abrams,et al.  Parts Outweigh the Whole (Word) in Unconscious Analysis of Meaning , 2000, Psychological science.

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

[14]  Robert M. Haralick,et al.  Feature normalization and likelihood-based similarity measures for image retrieval , 2001, Pattern Recognit. Lett..

[15]  C. Büchel,et al.  Event-Related fMRI Reveals Cortical Sites Involved in Contextual Sentence Integration , 2002, NeuroImage.

[16]  Nathalie Japkowicz,et al.  The class imbalance problem: A systematic study , 2002, Intell. Data Anal..

[17]  Eric Achten,et al.  Multilingualism: an fMRI study , 2003, NeuroImage.

[18]  Helen L Jamison,et al.  Morphology and the internal structure of words. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Yosef Grodzinsky,et al.  Neural correlates of syntactic movement: converging evidence from two fMRI experiments , 2004, NeuroImage.

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

[21]  Werner Greve,et al.  Masked affective priming by name letters: Evidence for a correspondence of explicit and implicit self-esteem , 2005 .

[22]  M. Jung-Beeman Bilateral brain processes for comprehending natural language , 2005, Trends in Cognitive Sciences.

[23]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[24]  Stanislas Dehaene,et al.  Subliminal Convergence of Kanji and Kana Words: Further Evidence for Functional Parcellation of the Posterior Temporal Cortex in Visual Word Perception , 2005, Journal of Cognitive Neuroscience.

[25]  N. Block Two neural correlates of consciousness , 2005, Trends in Cognitive Sciences.

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

[27]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

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

[29]  Nao Ninomiya,et al.  The 10th anniversary of journal of visualization , 2007, J. Vis..

[30]  Stanislas Dehaene,et al.  Task-specific change of unconscious neural priming in the cerebral language network , 2007, Proceedings of the National Academy of Sciences.

[31]  Sheng He,et al.  Processing of Invisible Stimuli: Advantage of Upright Faces and Recognizable Words in Overcoming Interocular Suppression , 2007, Psychological science.

[32]  S. Dehaene,et al.  Levels of processing during non-conscious perception: a critical review of visual masking , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  Michele T. Diaz,et al.  Unconscious Word Processing Engages a Distributed Network of Brain Regions , 2007, Journal of Cognitive Neuroscience.

[34]  R. Passingham,et al.  Unconscious Activation of the Cognitive Control System in the Human Prefrontal Cortex , 2007, The Journal of Neuroscience.

[35]  Stanislas Dehaene,et al.  Cerebral bases of subliminal and supraliminal priming during reading. , 2007, Cerebral cortex.

[36]  Janine D. Mendola,et al.  Eye dominance predicts fMRI signals in human retinotopic cortex , 2007, Neuroscience Letters.

[37]  Alfonso Caramazza,et al.  Unconscious processing dissociates along categorical lines , 2008, Proceedings of the National Academy of Sciences.

[38]  Raymond J. Dolan,et al.  fMRI Activity Patterns in Human LOC Carry Information about Object Exemplars within Category , 2008, Journal of Cognitive Neuroscience.

[39]  Axel Cleeremans,et al.  Measuring consciousness: relating behavioural and neurophysiological approaches , 2008, Trends in Cognitive Sciences.

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

[41]  K. R. Ridderinkhof,et al.  Frontal Cortex Mediates Unconsciously Triggered Inhibitory Control , 2008, The Journal of Neuroscience.

[42]  K. Shapiro,et al.  The contingent negative variation (CNV) event-related potential (ERP) predicts the attentional blink , 2008 .

[43]  J. R. Doyle Semantic activation without conscious identification in dichotic listening , parafoveal vision , and visual masking : A survey and appraisal , 2008 .

[44]  Sheng He,et al.  Semantic and subword priming during binocular suppression , 2009, Consciousness and Cognition.

[45]  Dirk B. Walther,et al.  Natural Scene Categories Revealed in Distributed Patterns of Activity in the Human Brain , 2009, The Journal of Neuroscience.

[46]  Miranda Scolari,et al.  Estimating the influence of attention on population codes in human visual cortex using voxel-based tuning functions , 2009, NeuroImage.

[47]  Sheng He,et al.  Seeing the invisible: The scope and limits of unconscious processing in binocular rivalry , 2008, Progress in Neurobiology.

[48]  John-Dylan Haynes,et al.  Decoding visual consciousness from human brain signals , 2009, Trends in Cognitive Sciences.

[49]  Bert Reynvoet,et al.  Mechanisms of masked priming: a meta-analysis. , 2009, Psychological bulletin.

[50]  Simon van Gaal,et al.  Unconscious Activation of the Prefrontal No-Go Network , 2010, The Journal of Neuroscience.

[51]  Nikolaus Kriegeskorte,et al.  Comparison of multivariate classifiers and response normalizations for pattern-information fMRI , 2010, NeuroImage.

[52]  V. Walsh,et al.  Subjective discriminability of invisibility: A framework for distinguishing perceptual and attentional failures of awareness , 2010, Consciousness and Cognition.

[53]  Emmanuel Dupoux,et al.  How Rich Is Consciousness? the Partial Awareness Hypothesis Opinion , 2022 .

[54]  Andrew D. Engell,et al.  Distributed representations of dynamic facial expressions in the superior temporal sulcus. , 2010, Journal of vision.

[55]  Daniel Ansari,et al.  Second revision : Supplementary Material Linking brain-wide multivoxel activation patterns to behaviour : examples from language and math , 2010 .

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

[57]  Tal Makovski,et al.  The visual attractor illusion. , 2010, Journal of vision.

[58]  Hanna Damasio,et al.  Predicting visual stimuli on the basis of activity in auditory cortices , 2010, Nature Neuroscience.

[59]  N. Kanwisher,et al.  New method for fMRI investigations of language: defining ROIs functionally in individual subjects. , 2010, Journal of neurophysiology.

[60]  Andrew T. Smith,et al.  The confounding effect of response amplitude on MVPA performance measures , 2011, NeuroImage.

[61]  Su-Ling Yeh,et al.  Accessing the meaning of invisible words , 2011, Consciousness and Cognition.

[62]  Bernard Mazoyer,et al.  What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis , 2011, NeuroImage.

[63]  S. Dehaene,et al.  The unique role of the visual word form area in reading , 2011, Trends in Cognitive Sciences.

[64]  Marlene Behrmann,et al.  Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis , 2011, Proceedings of the National Academy of Sciences.

[65]  Johannes J. Fahrenfort,et al.  Dissociable Brain Mechanisms Underlying the Conscious and Unconscious Control of Behavior , 2011, Journal of Cognitive Neuroscience.

[66]  Kara D. Federmeier,et al.  Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). , 2011, Annual review of psychology.

[67]  Randolph Blake,et al.  Journal Section: Behavior/systems/cognitive Title: Semantic Analysis Does Not Occur in the Absence of Awareness Induced by Interocular Suppression Abbreviated Title: No Semantic Processing during Interocular Suppression , 2022 .

[68]  Nancy Kanwisher,et al.  Functional specificity for high-level linguistic processing in the human brain , 2011, Proceedings of the National Academy of Sciences.

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

[70]  Pieter Moors,et al.  Using Interocular Suppression and EEG to Study Semantic Processing , 2012, The Journal of Neuroscience.

[71]  Sid Kouider,et al.  Nonconscious Influences from Emotional Faces: A Comparison of Visual Crowding, Masking, and Continuous Flash Suppression , 2012, Front. Psychology.

[72]  Sharon L. Thompson-Schill,et al.  The advantage of brief fMRI acquisition runs for multi-voxel pattern detection across runs , 2012, NeuroImage.

[73]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[74]  N. Kanwisher,et al.  Lexical and syntactic representations in the brain: An fMRI investigation with multi-voxel pattern analyses , 2011, Neuropsychologia.

[75]  V. Lamme,et al.  Unconscious High-Level Information Processing , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[76]  G. Yovel,et al.  Hierarchical Processing of Face Viewpoint in Human Visual Cortex , 2012, The Journal of Neuroscience.

[77]  Johannes Jacobus Fahrenfort,et al.  Neuronal integration in visual cortex elevates face category tuning to conscious face perception , 2012, Proceedings of the National Academy of Sciences.

[78]  Frank Tong,et al.  Relationship between BOLD amplitude and pattern classification of orientation-selective activity in the human visual cortex , 2012, NeuroImage.

[79]  Nir Levy,et al.  Reading and doing arithmetic nonconsciously , 2012, Proceedings of the National Academy of Sciences.

[80]  Helen J. Neville,et al.  The Human Brain Processes Syntax in the Absence of Conscious Awareness , 2013, The Journal of Neuroscience.

[81]  Scott D. Slotnick,et al.  The Visual Word Form Area , 2013 .

[82]  Marc N. Coutanche,et al.  Distinguishing Multi-voxel Patterns and Mean Activation: Why, How, and What Does It Tell Us? a Question of Spatial Frequency , 2022 .

[83]  Alfonso Caramazza,et al.  Affect of the unconscious: Visually suppressed angry faces modulate our decisions , 2012, Cognitive, Affective, & Behavioral Neuroscience.