Gamma-band activity reflects attentional guidance by facial expression

Abstract Facial expressions attract attention due to their motivational significance. Previous work focused on attentional biases towards threat‐related, fearful faces, although healthy participants tend to avoid mild threat. Growing evidence suggests that neuronal gamma (>30 Hz) and alpha‐band activity (8–12 Hz) play an important role in attentional selection, but it is unknown if such oscillatory activity is involved in the guidance of attention through facial expressions. Thus, in this magnetoencephalography (MEG) study we investigated whether attention is shifted towards or away from fearful faces and characterized the underlying neuronal activity in these frequency ranges in forty‐four healthy volunteers. We employed a covert spatial attention task using neutral and fearful faces as task‐irrelevant distractors and emotionally neutral Gabor patches as targets. Participants had to indicate the tilt direction of the target. Analysis of the neuronal data was restricted to the responses to target Gabor patches. We performed statistical analysis at the sensor level and used subsequent source reconstruction to localize the observed effects. Spatially selective attention effects in the alpha and gamma band were revealed in parieto‐occipital regions. We observed an attentional cost of processing the face distractors, as reflected in lower task performance on targets with short stimulus onset asynchrony (SOA <150 ms) between faces and targets. On the neuronal level, attentional orienting to face distractors led to enhanced gamma band activity in bilateral occipital and parietal regions, when fearful faces were presented in the same hemifield as targets, but only in short SOA trials. Our findings provide evidence that both top‐down and bottom‐up attentional biases are reflected in parieto‐occipital gamma‐band activity.

[1]  Geert Crombez,et al.  Attentional bias to threat: a perceptual accuracy approach. , 2008, Emotion.

[2]  J. Lisman,et al.  Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. , 2002, Cerebral cortex.

[3]  R. Dolan,et al.  Cholinergic Enhancement of Visual Attention and Neural Oscillations in the Human Brain , 2012, Current Biology.

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

[5]  C. MacLeod,et al.  Attentional bias in emotional disorders. , 1986, Journal of abnormal psychology.

[6]  Fanny Lachat,et al.  Watch Out! Magnetoencephalographic Evidence for Early Modulation of Attention Orienting by Fearful Gaze Cueing , 2012, PloS one.

[7]  G. V. Simpson,et al.  Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex , 2000, The Journal of Neuroscience.

[8]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[9]  Joachim Gross,et al.  Good practice for conducting and reporting MEG research , 2013, NeuroImage.

[10]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[11]  S. Rose Selective attention , 1992, Nature.

[12]  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.

[13]  K. Mogg,et al.  A cognitive-motivational analysis of anxiety. , 1998, Behaviour research and therapy.

[14]  M. Eysenck,et al.  Attentional bias to threat in clinical anxiety states , 1992 .

[15]  C. MacLeod,et al.  Attentional bias in emotional disorders. , 1986, Journal of abnormal psychology.

[16]  Inga M. Schepers,et al.  Altered Intrinsic Neuronal Interactions in the Visual Cortex of the Blind , 2013, The Journal of Neuroscience.

[17]  S. Langton,et al.  Attentional bias to angry faces using the dot-probe task? It depends when you look for it. , 2006, Behaviour research and therapy.

[18]  S. Yantis,et al.  Selective visual attention and perceptual coherence , 2006, Trends in Cognitive Sciences.

[19]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

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

[21]  Shwu-Lih Huang,et al.  Task-irrelevant angry faces capture attention in visual search while modulated by resources. , 2011, Emotion.

[22]  J. Kaiser,et al.  Activity in Human Visual and Parietal Cortex Reveals Object-Based Attention in Working Memory , 2015, The Journal of Neuroscience.

[23]  A. Engel,et al.  Neuronal Synchronization along the Dorsal Visual Pathway Reflects the Focus of Spatial Attention , 2008, Neuron.

[24]  G. Crombez,et al.  Selective attention to threat in the dot probe paradigm: differentiating vigilance and difficulty to disengage. , 2004, Behaviour research and therapy.

[25]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[26]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[27]  Gilles Pourtois,et al.  Neural systems for orienting attention to the location of threat signals: An event-related fMRI study , 2006, NeuroImage.

[28]  Natalie C. Ebner,et al.  FACES—A database of facial expressions in young, middle-aged, and older women and men: Development and validation , 2010, Behavior research methods.

[29]  K. Mogg,et al.  ATTENTIONAL BIASES FOR EMOTIONAL FACES , 1997 .

[30]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[31]  Seppo P. Ahlfors,et al.  Early Preferential Responses to Fear Stimuli in Human Right Dorsal Visual Stream - A Meg Study , 2016, Scientific Reports.

[32]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

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

[34]  J Gross,et al.  REPRINTS , 1962, The Lancet.

[35]  Carlos M. Hamamé,et al.  Selective attention modulates high-frequency activity in the face-processing network , 2014, Cortex.

[36]  Philippe Kahane,et al.  Efficient “Pop-Out” Visual Search Elicits Sustained Broadband Gamma Activity in the Dorsal Attention Network , 2012, The Journal of Neuroscience.

[37]  Reza Habib,et al.  Backward masked fearful faces enhance contralateral occipital cortical activity for visual targets within the spotlight of attention. , 2011, Social cognitive and affective neuroscience.

[38]  J. Yiend The effects of emotion on attention: A review of attentional processing of emotional information , 2010 .

[39]  E. Koster,et al.  Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review. , 2010, Clinical psychology review.

[40]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[41]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[42]  D. Thomson,et al.  Spectrum estimation and harmonic analysis , 1982, Proceedings of the IEEE.