A real-time marker of object-based attention in the human brain. A possible component of a “gate-keeping mechanism” performing late attentional selection in the Ventro-Lateral Prefrontal Cortex

The decision to process an incoming stimulus attentively - and to trigger a follow-up cascade of high-level processes - is strategic for the human brain as it becomes transiently unavailable to subsequent stimulus processing. In this study, we set to identify brain networks that carry out such evaluations. We therefore assessed the time-course of neural responses with intracerebral EEG in human patients during an attentional reading task, contrasting to-be-attended vs. to-be-ignored items. We measured High-Frequency Activity [50-150 Hz] as a proxy of population-level spiking activity and we identified a crucial component of a Gate-Keeping Mechanism bilateral in the mid-Ventro-Lateral Prefrontal Cortex (VLPFC), at the interplay of the Ventral and Dorsal Attention Networks, that selectively reacts before domain specialized cortical regions that engage in full stimulus analysis according to task demands.

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

[2]  P. Roelfsema,et al.  The threshold for conscious report: Signal loss and response bias in visual and frontal cortex , 2018, Science.

[3]  Jason M. Chein,et al.  Domain-general mechanisms of complex working memory span , 2011, NeuroImage.

[4]  Philippe Kahane,et al.  Invasive EEG in the definition of the seizure onset zone: depth electrodes , 2003 .

[5]  M. Eimer.  The neural basis of attentional control in visual search , 2014, Trends in Cognitive Sciences.

[6]  K Sekihara,et al.  NUTMEG: a neuromagnetic source reconstruction toolbox. , 2004, Neurology & clinical neurophysiology : NCN.

[7]  John R Anderson,et al.  An integrated theory of the mind. , 2004, Psychological review.

[8]  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.

[9]  Hans-Jochen Heinze,et al.  An electrophysiological dissociation of craving and stimulus-dependent attentional capture in smokers , 2016, Cognitive, Affective, & Behavioral Neuroscience.

[10]  Charles L. Folk,et al.  The structure of attentional control: contingent attentional capture by apparent motion, abrupt onset, and color , 1994 .

[11]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[12]  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.

[13]  J. Martinerie,et al.  Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony , 2001, Journal of Neuroscience Methods.

[14]  Denis Rivière,et al.  IntrAnat Electrodes: A Free Database and Visualization Software for Intracranial Electroencephalographic Data Processed for Case and Group Studies , 2018, Front. Neuroinform..

[15]  S. Yantis,et al.  On the distinction between visual salience and stimulus-driven attentional capture. , 1999, Journal of experimental psychology. Human perception and performance.

[16]  B. Baars,et al.  The Timing of the Cognitive Cycle , 2011, PloS one.

[17]  H. T. ten Donkelaar,et al.  Toward a Common Terminology for the Gyri and Sulci of the Human Cerebral Cortex , 2018, Front. Neuroanat..

[18]  T. Allison,et al.  Modulation of human extrastriate visual processing by selective attention to colours and words. , 1998, Brain : a journal of neurology.

[19]  P Kahane,et al.  Intracranial EEG and human brain mapping , 2003, Journal of Physiology-Paris.

[20]  N. Sigala,et al.  Dynamic Coding for Cognitive Control in Prefrontal Cortex , 2013, Neuron.

[21]  K. C. Anderson,et al.  Single neurons in prefrontal cortex encode abstract rules , 2001, Nature.

[22]  S. Yantis.  2. Attentional capture in vision , 1996 .

[23]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[24]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[25]  J. Duncan.  The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

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

[27]  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.

[28]  John Duncan,et al.  Coding of Visual, Auditory, Rule, and Response Information in the Brain: 10 Years of Multivoxel Pattern Analysis , 2016, Journal of Cognitive Neuroscience.

[29]  P. Morosan,et al.  Broca's Region: Novel Organizational Principles and Multiple Receptor Mapping , 2010, PLoS biology.

[30]  Steven J Luck,et al.  Capture versus suppression of attention by salient singletons: Electrophysiological evidence for an automatic attend-to-me signal , 2010, Attention, perception & psychophysics.

[31]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[32]  Juan R. Vidal,et al.  Transient Suppression of Broadband Gamma Power in the Default-Mode Network Is Correlated with Task Complexity and Subject Performance , 2011, The Journal of Neuroscience.

[33]  Gabriele Arnulfo,et al.  Phase and amplitude correlations in resting-state activity in human stereotactical EEG recordings , 2015, NeuroImage.

[34]  S. Wise,et al.  Rule-dependent neuronal activity in the prefrontal cortex , 1999, Experimental Brain Research.

[35]  R W Remington,et al.  The structure of attentional control: contingent attentional capture by apparent motion, abrupt onset, and color. , 1994, Journal of experimental psychology. Human perception and performance.

[36]  Juan R. Vidal,et al.  How Silent Is Silent Reading? Intracerebral Evidence for Top-Down Activation of Temporal Voice Areas during Reading , 2012, The Journal of Neuroscience.

[37]  Dominique Lamy,et al.  Effects of task relevance and stimulus-driven salience in feature-search mode. , 2004, Journal of experimental psychology. Human perception and performance.

[38]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[39]  Maro G. Machizawa,et al.  Neural activity predicts individual differences in visual working memory capacity , 2004, Nature.

[40]  S. Thorpe,et al.  The Time Course of Visual Processing: From Early Perception to Decision-Making , 2001, Journal of Cognitive Neuroscience.

[41]  Allen Newell,et al.  The model human processor: An engineering model of human performance. , 1986 .

[42]  J. Wolfe,et al.  Guided Search 2.0 A revised model of visual search , 1994, Psychonomic bulletin & review.

[43]  S. Kastner,et al.  Functional Specialization in the Attention Network. , 2020, Annual review of psychology.

[44]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[45]  S. Thorpe,et al.  The time course of visual processing: Backward masking and natural scene categorisation , 2005, Vision Research.

[46]  Karim Jerbi,et al.  ELAN: A Software Package for Analysis and Visualization of MEG, EEG, and LFP Signals , 2011, Comput. Intell. Neurosci..

[47]  H. Egeth,et al.  Overriding stimulus-driven attentional capture , 1994, Perception & psychophysics.

[48]  O. Bertrand,et al.  Oscillatory gamma-band (30-70 Hz) activity induced by a visual search task in humans. , 1997, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  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.

[50]  E. Macaluso,et al.  Dissociation of stimulus relevance and saliency factors during shifts of visuospatial attention. , 2007, Cerebral cortex.

[51]  J. Theeuwes,et al.  Attentional and oculomotor capture , 2001 .

[52]  Bradley S. Gibson,et al.  Stimulus-Driven Attentional Capture Is Contingent on Attentional Set for Displaywide Visual Features , 1998 .

[53]  Daniel J Mitchell,et al.  A Putative Multiple-Demand System in the Macaque Brain , 2016, The Journal of Neuroscience.

[54]  VanrullenRufin,et al.  The Time Course of Visual Processing: From Early Perception to Decision-Making , 2001 .

[55]  J. Pernier,et al.  Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans , 1997, The Journal of Neuroscience.

[56]  J. Theeuwes.  Top-down and bottom-up control of visual selection. , 2010, Acta psychologica.

[57]  J. Duncan,et al.  Visual search and stimulus similarity. , 1989, Psychological review.

[58]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[59]  P. Roelfsema,et al.  Different States in Visual Working Memory: When It Guides Attention and When It Does Not , 2022 .

[60]  John Duncan,et al.  Hierarchical coding for sequential task events in the monkey prefrontal cortex , 2008, Proceedings of the National Academy of Sciences.

[61]  Ramakrishna Chakravarthi,et al.  For whom the bell tolls: periodic reactivation of sensory cortex in the gamma band as a substrate of visual working memory maintenance , 2014, Front. Hum. Neurosci..

[62]  Martin Eimer,et al.  Attentional capture by task-irrelevant fearful faces is revealed by the N2pc component , 2007, Biological Psychology.

[63]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[64]  B. Gibson,et al.  Stimulus-driven attentional capture is contingent on attentional set for displaywide visual features. , 1998, Journal of experimental psychology. Human perception and performance.

[65]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[66]  K. Sakai.  Task set and prefrontal cortex. , 2008, Annual review of neuroscience.

[67]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

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