Attentional Bias to Briefly Presented Emotional Distractors Follows a Slow Time Course in Visual Cortex

A central controversy in the field of attention is how the brain deals with emotional distractors and to what extent they capture attentional processing resources reflexively due to their inherent significance for guidance of adaptive behavior and survival. Especially, the time course of competitive interactions in early visual areas and whether masking of briefly presented emotional stimuli can inhibit biasing of processing resources in these areas is currently unknown. We recorded frequency-tagged potentials evoked by a flickering target detection task in the foreground of briefly presented emotional or neutral pictures that were followed by a mask in human subjects. We observed greater competition for processing resources in early visual cortical areas with shortly presented emotional relative to neutral pictures ∼275 ms after picture offset. This was paralleled by a reduction of target detection rates in trials with emotional pictures ∼400 ms after picture offset. Our finding that briefly presented emotional distractors are able to bias attention well after their offset provides evidence for a rather slow feedback or reentrant neural competition mechanism for emotional distractors that continues after the offset of the emotional stimulus.

[1]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[2]  Peter J. Lang,et al.  Gaze Patterns When Looking at Emotional Pictures: Motivationally Biased Attention , 2004 .

[3]  Søren K. Andersen,et al.  Time course of affective bias in visual attention: Convergent evidence from steady-state visual evoked potentials and behavioral data , 2010, NeuroImage.

[4]  N. Trujillo-Barreto,et al.  3D Statistical Parametric Mapping of EEG Source Spectra by Means of Variable Resolution Electromagnetic Tomography (VARETA) , 2001, Clinical EEG.

[5]  Gilles Pourtois,et al.  Temporal precedence of emotion over attention modulations in the lateral amygdala: Intracranial ERP evidence from a patient with temporal lobe epilepsy , 2010, Cognitive, affective & behavioral neuroscience.

[6]  M. Bradley,et al.  Brain potentials in perception: picture complexity and emotional arousal. , 2007, Psychophysiology.

[7]  M. Eimer,et al.  The processing of emotional facial expression is gated by spatial attention: evidence from event-related brain potentials. , 2003, Brain research. Cognitive brain research.

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

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

[10]  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.

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

[12]  S. Yantis,et al.  Stimulus-driven attentional capture: evidence from equiluminant visual objects. , 1994, Journal of experimental psychology. Human perception and performance.

[13]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[14]  Andreas Keil,et al.  Time course of competition for visual processing resources between emotional pictures and foreground task. , 2008, Cerebral cortex.

[15]  Prashant Parikh A Theory of Communication , 2010 .

[16]  M. Junghöfer,et al.  The selective processing of briefly presented affective pictures: an ERP analysis. , 2004, Psychophysiology.

[17]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[18]  P. Lang International Affective Picture System (IAPS) : Technical Manual and Affective Ratings , 1995 .

[19]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[20]  François Mauguière,et al.  Early Amygdala Reaction to Fear Spreading in Occipital, Temporal, and Frontal Cortex A Depth Electrode ERP Study in Human , 2004, Neuron.

[21]  Steven A. Hillyard,et al.  Attention Facilitates Multiple Stimulus Features in Parallel in Human Visual Cortex , 2008, Current Biology.

[22]  T. Holroyd,et al.  Emotional Automaticity Is a Matter of Timing , 2010, The Journal of Neuroscience.

[23]  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.

[24]  Andreas Keil,et al.  Motivated attention in emotional picture processing is reflected by activity modulation in cortical attention networks , 2004, NeuroImage.

[25]  Christine L Larson,et al.  Stability of emotion-modulated startle during short and long picture presentation. , 2005, Psychophysiology.

[26]  D. Amaral,et al.  Synaptic organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey , 2005, The Journal of comparative neurology.

[27]  P. Lang,et al.  Re‐entrant projections modulate visual cortex in affective perception: Evidence from Granger causality analysis , 2009, Human brain mapping.

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

[29]  M. Bradley,et al.  Activation of the visual cortex in motivated attention. , 2003, Behavioral neuroscience.

[30]  Denis Fize,et al.  Speed of processing in the human visual system , 1996, Nature.

[31]  G R Loftus,et al.  Eye fixations and memory for emotional events. , 1991, Journal of experimental psychology. Learning, memory, and cognition.

[32]  Joseph E LeDoux The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1996 .

[33]  S. Paradiso The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[34]  D. Amaral,et al.  The organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey , 2005, The Journal of comparative neurology.

[35]  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.

[36]  A. Ohman,et al.  Emotion drives attention: detecting the snake in the grass. , 2001, Journal of experimental psychology. General.