Reward-associated features capture attention in the absence of awareness: Evidence from object-substitution masking

Reward-associated visual features have been shown to capture visual attention, evidenced in faster and more accurate behavioral performance, as well as in neural responses reflecting lateralized shifts of visual attention to those features. Specifically, the contralateral N2pc event-related-potential (ERP) component that reflects attentional shifting exhibits increased amplitude in response to task-relevant targets containing a reward-associated feature. In the present study, we examined the automaticity of such reward-association effects using object-substitution masking (OSM) in conjunction with MEG measures of visual attentional shifts. In OSM, a visual-search array is presented, with the target item to be detected indicated by a surrounding mask (here, four surrounding squares). Delaying the offset of the target-surrounding four-dot mask relative to the offset of the rest of the target/distracter array disrupts the viewer's awareness of the target (masked condition), whereas simultaneous offsets do not (unmasked condition). Here we manipulated whether the color of the OSM target was or was not of a previously reward-associated color. By tracking reward-associated enhancements of behavior and the N2pc in response to masked targets containing a previously rewarded or unrewarded feature, the automaticity of attentional capture by reward could be probed. We found an enhanced N2pc response to targets containing a previously reward-associated color feature. Moreover, this enhancement of the N2pc by reward did not differ between masking conditions, nor did it differ as a function of the apparent visibility of the target within the masked condition. Overall, these results underscore the automaticity of attentional capture by reward-associated features, and demonstrate the ability of feature-based reward associations to shape attentional capture and allocation outside of perceptual awareness.

[1]  Hans-Jochen Heinze,et al.  The Rapid Capture of Attention by Rewarded Objects , 2016, Journal of Cognitive Neuroscience.

[2]  Steven Yantis,et al.  Learned Value Magnifies Salience-Based Attentional Capture , 2011, PloS one.

[3]  Mika Koivisto,et al.  How Meaning Shapes Seeing , 2007, Psychological science.

[4]  Patryk A. Laurent,et al.  Value-driven attentional capture , 2011, Proceedings of the National Academy of Sciences.

[5]  Marty G. Woldorff,et al.  Neural processing stages during object-substitution masking and their relationship to perceptual awareness , 2013, Neuropsychologia.

[6]  Senqing Qi,et al.  Neural correlates of reward-driven attentional capture in visual search , 2013, Brain Research.

[7]  M. Fuchs,et al.  Linear and nonlinear current density reconstructions. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

[9]  Jesse J. Suh,et al.  Neural responses to subliminally presented cannabis and other emotionally evocative cues in cannabis-dependent individuals , 2013, Psychopharmacology.

[10]  L. Chelazzi,et al.  Visual Selective Attention and the Effects of Monetary Rewards , 2006, Psychological science.

[11]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[12]  Philip L. Smith,et al.  An integrated theory of attention and decision making in visual signal detection. , 2009, Psychological review.

[13]  M. Fuchs,et al.  An improved boundary element method for realistic volume-conductor modeling , 1998, IEEE Transactions on Biomedical Engineering.

[14]  L. Chelazzi,et al.  Behavioral/systems/cognitive Reward Changes Salience in Human Vision via the Anterior Cingulate , 2022 .

[15]  W. Zoest,et al.  Reward-associated stimuli capture the eyes in spite of strategic attentional set , 2013, Vision Research.

[16]  C. N. Boehler,et al.  Rapid recurrent processing gates awareness in primary visual cortex , 2008, Proceedings of the National Academy of Sciences.

[17]  Viola S. Störmer,et al.  Reward speeds up and increases consistency of visual selective attention: a lifespan comparison , 2014, Cognitive, affective & behavioral neuroscience.

[18]  C. N. Boehler,et al.  Reward- and Attention-related Biasing of Sensory Selection in Visual Cortex , 2014, Journal of Cognitive Neuroscience.

[19]  R. Desimone,et al.  Responses of Neurons in Inferior Temporal Cortex during Memory- Guided Visual Search , 1998 .

[20]  E. Reingold,et al.  Using direct and indirect measures to study perception without awareness , 1988, Perception & psychophysics.

[21]  J-M Hopf,et al.  Dynamics of feature binding during object-selective attention , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  G. Fink,et al.  The Neural Basis of Perceptual Hypothesis Generation and Testing , 2006, Journal of Cognitive Neuroscience.

[23]  G. Woodman,et al.  Dissociations Among Attention, Perception, and Awareness During Object-Substitution Masking , 2003, Psychological science.

[24]  Endel Põder,et al.  Attentional gating models of object substitution masking. , 2013, Journal of experimental psychology. General.

[25]  S. Luck,et al.  Neural sources of focused attention in visual search. , 2000, Cerebral cortex.

[26]  V. Lollo,et al.  Beyond the attentional blink: visual masking by object substitution. , 1998, Journal of experimental psychology. Human perception and performance.

[27]  Anne Treisman,et al.  Implicit Perception and Level of Processing in Object-Substitution Masking , 2009, Psychological science.

[28]  Nadim Joni Shah,et al.  The Neural Basis of Perceptual Hypothesis Generation and Testing , 2006, Journal of Cognitive Neuroscience.

[29]  M. Sarlo,et al.  The time course of implicit processing of facial features: An event-related potential study , 2011, Neuropsychologia.

[30]  Asaid Khateb,et al.  Electrophysiological evidence for early non-conscious processing of fearful facial expressions. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[31]  Yue-jia Luo,et al.  The time course of implicit processing of erotic pictures: An event-related potential study , 2011, Brain Research.

[32]  Jon Driver,et al.  Reward Priority of Visual Target Singletons Modulates Event-Related Potential Signatures of Attentional Selection , 2009, Psychological science.

[33]  G. R. Mangun,et al.  Form-From-Motion: MEG Evidence for Time Course and Processing Sequence , 2003, Journal of Cognitive Neuroscience.

[34]  Michael Pilling,et al.  What is being masked in object substitution masking? , 2006, Journal of experimental psychology. Human perception and performance.

[35]  Marie L. Smith,et al.  Rapid processing of emotional expressions without conscious awareness. , 2012, Cerebral cortex.

[36]  Sheng He,et al.  Dynamics of processing invisible faces in the brain: Automatic neural encoding of facial expression information , 2009, NeuroImage.

[37]  J. Enns,et al.  What’s new in visual masking? , 2000, Trends in Cognitive Sciences.

[38]  Patrik Pluchino,et al.  Object-substitution masking modulates spatial attention deployment and the encoding of information in visual short-term memory: insights from occipito-parietal ERP components. , 2011, Psychophysiology.

[39]  Ronald A. Rensink,et al.  Competition for consciousness among visual events: the psychophysics of reentrant visual processes. , 2000, Journal of experimental psychology. General.

[40]  L. Chelazzi,et al.  Rewards teach visual selective attention , 2013, Vision Research.

[41]  Geoffrey F. Woodman,et al.  Electrophysiological measurement of rapid shifts of attention during visual search , 1999, Nature.

[42]  S J Luck,et al.  Spatial filtering during visual search: evidence from human electrophysiology. , 1994, Journal of experimental psychology. Human perception and performance.