Neural repetition suppression in ventral occipito-temporal cortex occurs during conscious and unconscious processing of frequent stimuli

Stimulus repetition can produce neural response attenuation in stimulus-category selective networks within the occipito-temporal lobe. It is hypothesized that this neural suppression reflects the functional sharpening of local neuronal assemblies which boosts information processing efficiency. This neural suppression phenomenon has been mainly reported during conditions of conscious stimulus perception. The question remains whether frequent stimuli processed in the absence of conscious perception also induce repetition suppression in those specialized networks. Using rare intracranial EEG recordings in the ventral occipito-temporal cortex (VOTC) of human epileptic patients we investigated neural repetition suppression in conditions of conscious and unconscious visual processing of words. To this end, we used an orthogonal design manipulating respectively stimulus repetition (frequent vs. unique stimuli) and conscious perception (masked vs. unmasked stimuli). By measuring the temporal dynamics of high-frequency broadband gamma activity in VOTC and testing for main and interaction effects, we report that early processing of words in word-form selective networks exhibits a temporal cascade of modulations by stimulus repetition and masking: neuronal attenuation initially is observed in response to repeated words (irrespective of consciousness), that is followed by a second modulation contingent upon word reportability (irrespective of stimulus repetition). Later on (>300ms post-stimulus), a significant effect of conscious perception on the extent of repetition suppression was observed. The temporal dynamics of consciousness, the recognition memory processes and their interaction revealed in this study advance our understanding of their contributions to the neural mechanisms of word processing in VOTC.

[1]  S. Dehaene,et al.  Converging Intracranial Markers of Conscious Access , 2009, PLoS biology.

[2]  T. Allison,et al.  Word recognition in the human inferior temporal lobe , 1994, Nature.

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

[4]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[5]  Philippe Kahane,et al.  Direct Evidence for Two Different Neural Mechanisms for Reading Familiar and Unfamiliar Words: An Intra-Cerebral EEG Study , 2011, Front. Hum. Neurosci..

[6]  Juan R. Vidal,et al.  Long-Distance Amplitude Correlations in the High Gamma Band Reveal Segregation and Integration within the Reading Network , 2012, The Journal of Neuroscience.

[7]  Florent Aubry,et al.  Piecemeal recruitment of left-lateralized brain areas during reading: A spatio-functional account , 2008, NeuroImage.

[8]  Philippe Kahane,et al.  Watching brain TV and playing brain ball exploring novel BCI strategies using real-time analysis of human intracranial data. , 2009, International review of neurobiology.

[9]  Masaaki Nishida,et al.  Differential visually-induced gamma-oscillations in human cerebral cortex , 2009, NeuroImage.

[10]  Philippe Kahane,et al.  Efficient “Pop-Out” Visual Search Elicits Sustained Broadband Gamma Activity in the Dorsal Attention Network , 2012, The Journal of Neuroscience.

[11]  Philippe Kahane,et al.  Task‐related gamma‐band dynamics from an intracerebral perspective: Review and implications for surface EEG and MEG , 2009, Human brain mapping.

[12]  R. Rosenfeld Patients , 2012, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[13]  Richard N. A. Henson,et al.  Incongruent Abstract Stimulus–Response Bindings Result in Response Interference: fMRI and EEG Evidence from Visual Object Classification Priming , 2012, Journal of Cognitive Neuroscience.

[14]  Tony Ro,et al.  Unconscious Priming Requires Early Visual Cortex at Specific Temporal Phases of Processing , 2013, Journal of Cognitive Neuroscience.

[15]  C. Price,et al.  The Interactive Account of ventral occipitotemporal contributions to reading , 2011, Trends in Cognitive Sciences.

[16]  Robert Oostenveld,et al.  Alpha-band suppression in the visual word form area as a functional bottleneck to consciousness , 2013, NeuroImage.

[17]  Philippe Kahane,et al.  A Blueprint for Real-Time Functional Mapping via Human Intracranial Recordings , 2007, PloS one.

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

[19]  Philippe Kahane,et al.  The neural bases of attentive reading , 2008, Human brain mapping.

[20]  Juan R. Vidal,et al.  Category-Specific Visual Responses: An Intracranial Study Comparing Gamma, Beta, Alpha, and ERP Response Selectivity , 2010, Front. Hum. Neurosci..

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

[22]  Philippe Kahane,et al.  Turning Visual Shapes into Sounds: Early Stages of Reading Acquisition , 2022 .

[23]  Michael J. Constantino,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008 .

[24]  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.

[25]  Laurie S. Glezer,et al.  Evidence for Highly Selective Neuronal Tuning to Whole Words in the “Visual Word Form Area” , 2009, Neuron.

[26]  R. Henson,et al.  Multiple levels of visual object constancy revealed by event-related fMRI of repetition priming , 2002, Nature Neuroscience.

[27]  Anders M. Dale,et al.  Multimodal imaging of repetition priming: Using fMRI, MEG, and intracranial EEG to reveal spatiotemporal profiles of word processing , 2010, NeuroImage.

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

[29]  Philippe Kahane,et al.  Exploring the electrophysiological correlates of the default ‐ mode network with intracerebral EEG , 2022 .

[30]  Christian J Fiebach,et al.  Neuronal Mechanisms of Repetition Priming in Occipitotemporal Cortex: Spatiotemporal Evidence from Functional Magnetic Resonance Imaging and Electroencephalography , 2005, The Journal of Neuroscience.

[31]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[32]  Catherine Tallon-Baudry,et al.  The many faces of the gamma band response to complex visual stimuli , 2005, NeuroImage.

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

[34]  O. Bertrand,et al.  Relationship between task‐related gamma oscillations and BOLD signal: New insights from combined fMRI and intracranial EEG , 2007, Human brain mapping.

[35]  J. M. Lina,et al.  Recording and analysis techniques for high-frequency oscillations , 2012, Progress in Neurobiology.

[36]  Brian Litt,et al.  Repeated stimuli elicit diminished high-gamma electrocorticographic responses , 2014, NeuroImage.

[37]  S. Dehaene,et al.  The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. , 2001, Cerebral cortex.

[38]  Ferath Kherif,et al.  Automatic Top-Down Processing Explains Common Left Occipito-Temporal Responses to Visual Words and Objects , 2010, Cerebral cortex.

[39]  David Badre,et al.  Multiple forms of learning yield temporally distinct electrophysiological repetition effects. , 2010, Cerebral cortex.

[40]  Nikolai Axmacher,et al.  Local Category-Specific Gamma Band Responses in the Visual Cortex Do Not Reflect Conscious Perception , 2012, The Journal of Neuroscience.

[41]  Ueli Rutishauser,et al.  Single-Trial Learning of Novel Stimuli by Individual Neurons of the Human Hippocampus-Amygdala Complex , 2006, Neuron.

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

[43]  R. Henson,et al.  Priming, response learning and repetition suppression , 2008, Neuropsychologia.

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

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

[46]  E. Halgren,et al.  High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research , 2012, Progress in Neurobiology.

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

[48]  T. Shallice,et al.  Neuroimaging evidence for dissociable forms of repetition priming. , 2000, Science.

[49]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[50]  William D. Marslen-Wilson,et al.  The time course of visual word recognition as revealed by linear regression analysis of ERP data , 2006, NeuroImage.

[51]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

[52]  Matthias M. Müller,et al.  Oscillatory brain activity dissociates between associative stimulus content in a repetition priming task in the human EEG. , 2004, Cerebral cortex.

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

[54]  Alice Mado Proverbio,et al.  From Orthography to Phonetics: ERP Measures of Grapheme-to-Phoneme Conversion Mechanisms in Reading , 2004, Journal of Cognitive Neuroscience.

[55]  Matthias M. Müller,et al.  Modulation of oscillatory brain activity and evoked potentials in a repetition priming task in the human EEG , 2004, The European journal of neuroscience.

[56]  Philippe Kahane,et al.  Dejerine's reading area revisited with intracranial EEG , 2013, Neurology.

[57]  Philippe Kahane,et al.  Reading the mind's eye: Online detection of visuo-spatial working memory and visual imagery in the inferior temporal lobe , 2012, NeuroImage.

[58]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[59]  Moqian Tian,et al.  Top-Down Processing of Symbolic Meanings Modulates the Visual Word Form Area , 2012, The Journal of Neuroscience.

[60]  Carson C. Chow,et al.  Repetition priming and repetition suppression: A case for enhanced efficiency through neural synchronization , 2012, Cognitive neuroscience.

[61]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.