Time matters: Feature-specific prioritization follows feature integration in visual object processing

Objects represent a fundamental selection unit of visual attention. However, at odds with the integrated competition account, our recent study demonstrated that attentional facilitation of constituent features does not spread automatically within an object, but instead depends on the specific task relevance of each feature. Here, we employed a novel experimental design, allowing simultaneous electrophysiological measurements of the allocation of attention to two distinct features (rotation and color) within one object (a square) during both trial-wise and block-wise cued shifts of attention. This was possible through the presentation of a square that evokes two distinct steady-state visual evoked potentials (SSVEPs) for its rotation and its color changes, respectively. Given the continuous oscillatory nature of SSVEPs, we were able to investigate the time course of neural activity in the early visual cortex of the human brain when subjects attended to one of the two features, compared to when the whole object was attended. This approach enabled us to uncover feature-based mechanisms of attention within one object, as well as their interaction with object-based mechanisms. Both behavioral and electrophysiological results indicate a biphasic process composed of an early transient integration of the constituent object features, followed by sustained mechanisms of feature selection with amplification of the to-be-attended feature, followed temporally by suppression of the to-be-ignored feature.

[1]  Dennis Gabor,et al.  Theory of communication , 1946 .

[2]  Matthias M. Müller,et al.  Bringing color to emotion: The influence of color on attentional bias to briefly presented emotional images , 2017, Cognitive, affective & behavioral neuroscience.

[3]  S. Luck,et al.  Attention to Features Precedes Attention to Locations in Visual Search: Evidence from Electromagnetic Brain Responses in Humans , 2004, The Journal of Neuroscience.

[4]  John H. R. Maunsell,et al.  Feature-based attention in visual cortex , 2006, Trends in Neurosciences.

[5]  Jeffrey N. Rouder,et al.  Bayesian t tests for accepting and rejecting the null hypothesis , 2009, Psychonomic bulletin & review.

[6]  J. Duncan Selective attention and the organization of visual information , 1984 .

[7]  Matthias M. Müller,et al.  Attentional modulation of the human somatosensory evoked potential in a trial-by-trial spatial cueing and sustained spatial attention task measured with high density 128 channels EEG. , 2004, Brain research. Cognitive brain research.

[8]  A. Kreiter,et al.  Attentional spreading to task-irrelevant object features: experimental support and a 3-step model of attention for object-based selection and feature-based processing modulation , 2014, Front. Hum. Neurosci..

[9]  Hans-Jochen Heinze,et al.  Object-based attention involves the sequential activation of feature-specific cortical modules , 2014, Nature Neuroscience.

[10]  J. Duncan,et al.  The Slow Time-Course of Visual Attention , 1996, Cognitive Psychology.

[11]  Hans-Jochen Heinze,et al.  Attention to adjacent and separate positions in space: An electrophysiological analysis , 1994, Perception & psychophysics.

[12]  Sean T. Stevens,et al.  Comparing the time course and efficacy of spatial and feature-based attention , 2007, Vision Research.

[13]  G. Mangun Neural mechanisms of visual selective attention. , 1995, Psychophysiology.

[14]  Hedderik van Rijn,et al.  Dissociable mechanisms underlying individual differences in visual working memory capacity , 2014, NeuroImage.

[15]  S. Yantis,et al.  Cortical mechanisms of space-based and object-based attentional control , 2003, Current Opinion in Neurobiology.

[16]  H Stanislaw,et al.  Calculation of signal detection theory measures , 1999, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[17]  B. Scholl Objects and attention: the state of the art , 2001, Cognition.

[18]  Matthias M. Müller,et al.  Selective Attention to Task-Irrelevant Emotional Distractors Is Unaffected by the Perceptual Load Associated with a Foreground Task , 2012, PloS one.

[19]  Matthias M. Müller Location and features of instructive spatial cues do not influence the time course of covert shifts of visual spatial attention , 2008, Biological Psychology.

[20]  S. Treue Neural correlates of attention in primate visual cortex , 2001, Trends in Neurosciences.

[21]  R. M. Boynton,et al.  Comparison of four methods of heterochromatic photometry. , 1972, Journal of the Optical Society of America.

[22]  D. Spinelli,et al.  Spatiotemporal analysis of the cortical sources of the steady‐state visual evoked potential , 2007, Human brain mapping.

[23]  Matthias M. Müller,et al.  Attentional Facilitation of Constituent Features of an Object Does Not Spread Automatically along Object-defining Cortical Boundaries , 2019, Journal of Cognitive Neuroscience.

[24]  H. Müller,et al.  Dimension-based visual attention modulates dual-judgment accuracy in Duncan's (1984) one- versus two-object report paradigm. , 2000, Journal of experimental psychology. Human perception and performance.

[25]  S. A. Hillyard,et al.  Sustained division of the attentional spotlight , 2003, Nature.

[26]  D. Alanallport Parallel encoding within and between elementary stimulus dimensions , 1971 .

[27]  Yaoda Xu,et al.  The Neural Fate of Task-Irrelevant Features in Object-Based Processing , 2010, The Journal of Neuroscience.

[28]  M. Valdés-Sosa,et al.  Switching Attention without Shifting the Spotlight: Object-Based Attentional Modulation of Brain Potentials , 1998, Journal of Cognitive Neuroscience.

[29]  Jeffrey N. Rouder,et al.  Bayes factor approaches for testing interval null hypotheses. , 2011, Psychological methods.

[30]  H. Jeffreys,et al.  Theory of probability , 1896 .

[31]  S. Yantis,et al.  Visual attention: control, representation, and time course. , 1997, Annual review of psychology.

[32]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[33]  Michael S. Pratte,et al.  Using MCMC chain outputs to efficiently estimate Bayes factors , 2011 .

[34]  S. Andersen,et al.  Behavioral performance follows the time course of neural facilitation and suppression during cued shifts of feature-selective attention , 2010, Proceedings of the National Academy of Sciences.

[35]  G. Woodman,et al.  Selective storage and maintenance of an object’s features in visual working memory , 2008, Psychonomic bulletin & review.

[36]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[37]  Søren K. Andersen,et al.  Global Enhancement but Local Suppression in Feature-based Attention , 2016, Journal of Cognitive Neuroscience.

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

[39]  G. R Mangun,et al.  Shifting visual attention in space: an electrophysiological analysis using high spatial resolution mapping , 2000, Clinical Neurophysiology.

[40]  Jeffrey N. Rouder,et al.  Default Bayes factors for ANOVA designs , 2012 .

[41]  P. Roelfsema Cortical algorithms for perceptual grouping. , 2006, Annual review of neuroscience.

[42]  Leonardo Chelazzi,et al.  Selective Attention to Specific Features within Objects: Behavioral and Electrophysiological Evidence , 2006, Journal of Cognitive Neuroscience.

[43]  Søren K. Andersen,et al.  Attentional bias of competitive interactions in neuronal networks of early visual processing in the human brain , 2008, NeuroImage.

[44]  M. Eimer “Sensory gating” as a mechanism for visuospatial orienting: Electrophysiological evidence from trial-by-trial cuing experiments , 1994, Perception & psychophysics.

[45]  E. Macaluso,et al.  fMRI correlates of object-based attentional facilitation vs. suppression of irrelevant stimuli, dependent on global grouping and endogenous cueing , 2013, Front. Integr. Neurosci..

[46]  Jens Schwarzbach,et al.  Control of object-based attention in human cortex. , 2004, Cerebral cortex.

[47]  B. Rockstroh,et al.  Statistical control of artifacts in dense array EEG/MEG studies. , 2000, Psychophysiology.

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

[49]  S A Hillyard,et al.  Feature-selective attention enhances color signals in early visual areas of the human brain , 2006, Proceedings of the National Academy of Sciences.

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

[51]  Matthias M. Müller,et al.  Sustained division of spatial attention to multiple locations within one hemifield , 2007, Neuroscience Letters.

[52]  S. Hillyard,et al.  Spatio-temporal analysis of feature-based attention. , 2007, Cerebral cortex.

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

[54]  Edward F. Ester,et al.  PSYCHOLOGICAL SCIENCE Research Article Stimulus-Specific Delay Activity in Human Primary Visual Cortex , 2022 .

[55]  J. Gallant,et al.  Time Course of Attention Reveals Different Mechanisms for Spatial and Feature-Based Attention in Area V4 , 2005, Neuron.

[56]  E. Vogel,et al.  Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[57]  Matthias M. Müller,et al.  The time course of cortical facilitation during cued shifts of spatial attention , 1998, Nature Neuroscience.