Decoding of task-relevant and task-irrelevant intracranial EEG representations

Natural stimuli consist of multiple properties. However, not all of these properties are equally relevant in a given situation. In this study, we applied multivariate classification algorithms to intracranial electroencephalography data of human epilepsy patients performing an auditory Stroop task. This allowed us to identify neuronal representations of task-relevant and irrelevant pitch and semantic information of spoken words in a subset of patients. When properties were relevant, representations could be detected after about 350ms after stimulus onset. When irrelevant, the association with gamma power differed for these properties. Patients with more reliable representations of irrelevant pitch showed increased gamma band activity (35-64Hz), suggesting that attentional resources allow an increase in gamma power in some but not all patients. This effect was not observed for irrelevant semantics, possibly because the more automatic processing of this property allowed for less variation in free resources. Processing of different properties of the same stimulus seems therefore to be dependent on the characteristics of the property.

[1]  Anina N. Rich,et al.  Attention enhances multi-voxel representation of novel objects in frontal, parietal and visual cortices , 2015, NeuroImage.

[2]  Mannes Poel,et al.  Online decoding of object‐based attention using real‐time fMRI , 2014, The European journal of neuroscience.

[3]  C Pantev,et al.  Right hemispheric laterality of human 40 Hz auditory steady-state responses. , 2005, Cerebral cortex.

[4]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[5]  Robert J. Zatorre,et al.  Neural substrates for dividing and focusing attention between simultaneous auditory and visual events , 2006, NeuroImage.

[6]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[7]  S. Hillyard,et al.  Modulation of early auditory processing during selective listening to rapidly presented tones. , 1991, Electroencephalography and clinical neurophysiology.

[8]  Gareth R. Barnes,et al.  Gamma band pitch responses in human auditory cortex measured with magnetoencephalography , 2012, NeuroImage.

[9]  Daniel J. Acheson,et al.  Increased Alpha-Band Power during the Retention of Shapes and Shape-Location Associations in Visual Short-Term Memory , 2011, Front. Psychology.

[10]  Marc Schönwiesner,et al.  Mapping Human Pitch Representation in a Distributed System Using Depth-Electrode Recordings and Modeling , 2012, The Journal of Neuroscience.

[11]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[12]  F. Tong,et al.  Decoding Seen and Attended Motion Directions from Activity in the Human Visual Cortex , 2006, Current Biology.

[13]  R. D. Hienz,et al.  Single-unit activity in the auditory cortex of monkeys selectively attending left vs. right ear stimuli , 1978, Brain Research.

[14]  Edward E. Smith,et al.  Attention Enhances the Neural Processing of Relevant Features and Suppresses the Processing of Irrelevant Features in Humans: A Functional Magnetic Resonance Imaging Study of the Stroop Task , 2008, The Journal of Neuroscience.

[15]  Moritz Grosse-Wentrup,et al.  Multisubject Learning for Common Spatial Patterns in Motor-Imagery BCI , 2011, Comput. Intell. Neurosci..

[16]  Philippe Kahane,et al.  High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex , 2005, NeuroImage.

[17]  B. Balas,et al.  Personal Familiarity Influences the Processing of Upright and Inverted Faces in Infants , 2009, Front. Hum. Neurosci..

[18]  Dwight J. Kravitz,et al.  Task context impacts visual object processing differentially across the cortex , 2014, Proceedings of the National Academy of Sciences.

[19]  Yoko Hoshi,et al.  Attention induces reciprocal activity in the human somatosensory cortex enhancing relevant- and suppressing irrelevant inputs from fingers , 2005, Clinical Neurophysiology.

[20]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[21]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[22]  Nikolai Axmacher,et al.  Activation of the caudal anterior cingulate cortex due to task‐related interference in an auditory Stroop paradigm , 2009, Human brain mapping.

[23]  O. Bertrand,et al.  Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. , 2005, Cerebral cortex.

[24]  W. Klimesch Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[25]  Michael A. Pitts,et al.  Gamma band activity and the P3 reflect post-perceptual processes, not visual awareness , 2014, NeuroImage.

[26]  Katrin Krumbholz,et al.  Feature- and Object-based Attentional Modulation in the Human Auditory Where Pathway , 2007, Journal of Cognitive Neuroscience.

[27]  Jochen Kaiser,et al.  Effects of feature-selective attention on auditory pattern and location processing , 2008, NeuroImage.

[28]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception , 2001, Clinical Neurophysiology.

[29]  R. VanRullen,et al.  An oscillatory mechanism for prioritizing salient unattended stimuli , 2012, Trends in Cognitive Sciences.

[30]  Rafael Malach,et al.  Spatial and Object-Based Attention Modulates Broadband High-Frequency Responses across the Human Visual Cortical Hierarchy , 2013, The Journal of Neuroscience.

[31]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.

[32]  Keiji Tanaka,et al.  Conflict-induced behavioural adjustment: a clue to the executive functions of the prefrontal cortex , 2009, Nature Reviews Neuroscience.

[33]  Werner Lutzenberger,et al.  Reciprocal modulation of neuromagnetic induced gamma activity by attention in the human visual and auditory cortex , 2004, NeuroImage.

[34]  Christian J. Sumner,et al.  Examining the role of frequency specificity in the enhancement and suppression of human cortical activity by auditory selective attention , 2009, Hearing Research.

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

[36]  Jasna Martinovic,et al.  Induced Gamma-band Activity Elicited by Visual Representation of Unattended Objects , 2009, Journal of Cognitive Neuroscience.

[37]  J. Downar,et al.  The Effect of Task Relevance on the Cortical Response to Changes in Visual and Auditory Stimuli: An Event-Related fMRI Study , 2001, NeuroImage.

[38]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[39]  Juha Salmi,et al.  Selective attention to sound location or pitch studied with fMRI , 2006, Brain Research.

[40]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

[41]  P. Fries,et al.  Is synchronized neuronal gamma activity relevant for selective attention? , 2003, Brain Research Reviews.

[42]  Wolfgang Klimesch,et al.  Alpha Oscillations and Early Stages of Visual Encoding , 2011, Front. Psychology.

[43]  Janneke F. M. Jehee,et al.  Attention Improves Encoding of Task-Relevant Features in the Human Visual Cortex , 2011, The Journal of Neuroscience.

[44]  Wolfgang Teder,et al.  Auditory attention and selective input modulation: A topographical ERP study , 1992, Neuroreport.

[45]  Simon Hanslmayr,et al.  Neural Communication Patterns Underlying Conflict Detection, Resolution, and Adaptation , 2014, The Journal of Neuroscience.

[46]  G. Mangun,et al.  Top-down Modulation of Neural Activity in Anticipatory Visual Attention: Control Mechanisms Revealed by Simultaneous EEG-fMRI. , 2014, Cerebral cortex.