Affective facilitation of early visual cortex during rapid picture presentation at 6 and 15 Hz.

The steady-state visual evoked potential (SSVEP), a neurophysiological marker of attentional resource allocation with its generators in early visual cortex, exhibits enhanced amplitude for emotional compared to neutral complex pictures. Emotional cue extraction for complex images is linked to the N1-EPN complex with a peak latency of ∼140-160 ms. We tested whether neural facilitation in early visual cortex with affective pictures requires emotional cue extraction of individual images, even when a stream of images of the same valence category is presented. Images were shown at either 6 Hz (167 ms, allowing for extraction) or 15 Hz (67 ms per image, causing disruption of processing by the following image). Results showed SSVEP amplitude enhancement for emotional compared to neutral images at a presentation rate of 6 Hz but no differences at 15 Hz. This was not due to featural differences between the two valence categories. Results strongly suggest that individual images need to be displayed for sufficient time allowing for emotional cue extraction to drive affective neural modulation in early visual cortex.

[1]  Markus Junghöfer,et al.  The selective processing of emotional visual stimuli while detecting auditory targets: An ERP analysis , 2008, Brain Research.

[2]  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.

[3]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[4]  M. Bradley,et al.  Fleeting images: a new look at early emotion discrimination. , 2001, Psychophysiology.

[5]  Jonas K. Olofsson,et al.  Affective picture processing: An integrative review of ERP findings , 2008, Biological Psychology.

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

[7]  R. Bakeman Recommended effect size statistics for repeated measures designs , 2005, Behavior research methods.

[8]  S. Hillyard,et al.  Selective attention to stimulus location modulates the steady-state visual evoked potential. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[9]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[10]  James W. Tanaka,et al.  The SHINE toolbox for controlling low-level image properties , 2010 .

[11]  M. Bradley,et al.  Electrocortical and electrodermal responses covary as a function of emotional arousal: a single-trial analysis. , 2008, Psychophysiology.

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

[13]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[14]  Bruno Rossion,et al.  Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170 , 2008, NeuroImage.

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

[16]  Karl R Gegenfurtner,et al.  The dynamics of visual pattern masking in natural scene processing: a magnetoencephalography study. , 2005, Journal of vision.

[17]  Andreas Keil,et al.  Additive effects of emotional content and spatial selective attention on electrocortical facilitation. , 2005, Cerebral cortex.

[18]  Andreas Keil,et al.  Parallel processing of affective visual stimuli. , 2009, Psychophysiology.

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

[20]  K. Scherer,et al.  The Geneva affective picture database (GAPED): a new 730-picture database focusing on valence and normative significance , 2011, Behavior research methods.

[21]  Patrik Vuilleumier,et al.  Emotional Attention , 2009 .

[22]  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.

[23]  Matthias M. Müller,et al.  Effects of spatial selective attention on the steady-state visual evoked potential in the 20-28 Hz range. , 1998, Brain research. Cognitive brain research.

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

[25]  Greg O. Horne,et al.  Controlling low-level image properties: The SHINE toolbox , 2010, Behavior research methods.

[26]  Thom Baguley,et al.  Serious stats: a guide to advanced statistics for the behavioral sciences , 2012 .

[27]  Antonio Schettino,et al.  rain mechanisms for emotional influences on perception and attention : hat is magic and what is not , 2012 .

[28]  Markus Junghöfer,et al.  Fleeting images: rapid affect discrimination in the visual cortex , 2006, Neuroreport.

[29]  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.

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

[31]  Maurizio Codispoti,et al.  Unmasking emotion: exposure duration and emotional engagement. , 2009, Psychophysiology.

[32]  Matthias M. Müller,et al.  Early modulation of visual perception by emotional arousal: Evidence from steady-state visual evoked brain potentials , 2003, Cognitive, affective & behavioral neuroscience.

[33]  Matthias M Müller,et al.  Attentional Bias to Briefly Presented Emotional Distractors Follows a Slow Time Course in Visual Cortex , 2011, The Journal of Neuroscience.

[34]  A. Norcia,et al.  The 6Hz fundamental stimulation frequency rate for individual face discrimination in the right occipito-temporal cortex , 2013, Neuropsychologia.

[35]  N. Kanwisher,et al.  PSYCHOLOGICAL SCIENCE Research Article Visual Recognition As Soon as You Know It Is There, You Know What It Is , 2022 .

[36]  Søren K. Andersen,et al.  Effects of Feature-selective and Spatial Attention at Different Stages of Visual Processing , 2011, Journal of Cognitive Neuroscience.

[37]  Matthias M. Müller,et al.  Slow biasing of processing resources in early visual cortex is preceded by emotional cue extraction in emotion–attention competition , 2014, Human brain mapping.

[38]  A. Cichocki,et al.  Steady-state visually evoked potentials: Focus on essential paradigms and future perspectives , 2010, Progress in Neurobiology.

[39]  M. Bradley,et al.  Rapid picture presentation and affective engagement. , 2006, Emotion.

[40]  J. Driver,et al.  Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  D. Regan Human brain electrophysiology: Evoked potentials and evoked magnetic fields in science and medicine , 1989 .

[42]  Christian Keysers,et al.  Visual masking and RSVP reveal neural competition , 2002, Trends in Cognitive Sciences.

[43]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[44]  P. Lang International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[45]  Markus Junghöfer,et al.  Rapid picture processing: affective primes and targets. , 2007, Psychophysiology.

[46]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

[47]  M. Junghöfer,et al.  Emotion and attention: event-related brain potential studies. , 2006, Progress in brain research.

[48]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[49]  J. Algina,et al.  Generalized eta and omega squared statistics: measures of effect size for some common research designs. , 2003, Psychological methods.

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

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

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

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

[54]  S. Wiens,et al.  Directed attention reduces processing of emotional distracters irrespective of valence and arousal level , 2013, Biological Psychology.

[55]  Matthias M. Müller,et al.  Concurrent recording of steady-state and transient event-related potentials as indices of visual-spatial selective attention , 2000, Clinical Neurophysiology.

[56]  Anna Weinberg,et al.  Beyond good and evil: the time-course of neural activity elicited by specific picture content. , 2010, Emotion.

[57]  L. Deouell,et al.  STRUCTURAL ENCODING AND IDENTIFICATION IN FACE PROCESSING: ERP EVIDENCE FOR SEPARATE MECHANISMS , 2000, Cognitive neuropsychology.

[58]  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.

[59]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[60]  Andreas Keil,et al.  The Timing of Emotional Discrimination in Human Amygdala and Ventral Visual Cortex , 2009, The Journal of Neuroscience.