Selective visual attention to emotional words: Early parallel frontal and visual activations followed by interactive effects in visual cortex

Human brains spontaneously differentiate between various emotional and neutral stimuli, including written words whose emotional quality is symbolic. In the electroencephalogram (EEG), emotional–neutral processing differences are typically reflected in the early posterior negativity (EPN, 200–300 ms) and the late positive potential (LPP, 400–700 ms). These components are also enlarged by task‐driven visual attention, supporting the assumption that emotional content naturally drives attention. Still, the spatio‐temporal dynamics of interactions between emotional stimulus content and task‐driven attention remain to be specified. Here, we examine this issue in visual word processing. Participants attended to negative, neutral, or positive nouns while high‐density EEG was recorded. Emotional content and top‐down attention both amplified the EPN component in parallel. On the LPP, by contrast, emotion and attention interacted: Explicit attention to emotional words led to a substantially larger amplitude increase than did explicit attention to neutral words. Source analysis revealed early parallel effects of emotion and attention in bilateral visual cortex and a later interaction of both in right visual cortex. Distinct effects of attention were found in inferior, middle and superior frontal, paracentral, and parietal areas, as well as in the anterior cingulate cortex (ACC). Results specify separate and shared mechanisms of emotion and attention at distinct processing stages. Hum Brain Mapp 37:3575–3587, 2016. © 2016 Wiley Periodicals, Inc.

[1]  Andreas Keil,et al.  Emotional perception: Correspondence of early and late event-related potentials with cortical and subcortical functional MRI , 2013, Biological Psychology.

[2]  E. Stern,et al.  Linguistic threat activates the human amygdala. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[4]  J. Kissler,et al.  Emotion and attention in visual word processing—An ERP study , 2009, Biological Psychology.

[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]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

[7]  Markus Junghöfer,et al.  The categorization of natural scenes: Brain attention networks revealed by dense sensor ERPs , 2006, NeuroImage.

[8]  Michèle Fabre-Thorpe,et al.  Interaction of top-down and bottom-up processing in the fast visual analysis of natural scenes. , 2004, Brain research. Cognitive brain research.

[9]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[10]  G. Pourtois,et al.  Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging , 2007, Neuropsychologia.

[11]  Theodore P. Zanto,et al.  Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory , 2011, Nature Neuroscience.

[12]  Harold Goodglass,et al.  Aphasic Reading and Writing: Possible Evidence for Right Hemisphere Participation , 1982, Cortex.

[13]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[14]  A. Jacobs,et al.  On pleasure and thrill: The interplay between arousal and valence during visual word recognition , 2014, Brain and Language.

[15]  Sebastian Schindler,et al.  It’s all in your head – how anticipating evaluation affects the processing of emotional trait adjectives , 2014, Front. Psychol..

[16]  Christoph M. Michel,et al.  Electrical neuroimaging reveals early generator modulation to emotional words , 2004, NeuroImage.

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

[18]  Mahzarin R. Banaji,et al.  Perspectivism in Social Psychology: The Yin and Yang of Scientific Progress , 2004 .

[19]  J. Cacioppo Asymmetries in affect-laden information processing. , 2004 .

[20]  Lars Kuchinke,et al.  Incidental effects of emotional valence in single word processing: An fMRI study , 2005, NeuroImage.

[21]  Joseph T. Devlin,et al.  Orienting attention to semantic categories , 2006, NeuroImage.

[22]  R. Deichmann,et al.  Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. , 2008, Cerebral cortex.

[23]  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.

[24]  Matthias M. Müller,et al.  Emotional words facilitate lexical but not early visual processing , 2015, BMC Neuroscience.

[25]  G. Kuperberg,et al.  Vivid: How valence and arousal influence word processing under different task demands , 2016, Cognitive, Affective, & Behavioral Neuroscience.

[26]  E. Miller,et al.  Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices , 2007, Science.

[27]  P. Pauli,et al.  Raised Middle-Finger: Electrocortical Correlates of Social Conditioning with Nonverbal Affective Gestures , 2014, PloS one.

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

[29]  M. Junghöfer,et al.  The facilitated processing of threatening faces: an ERP analysis. , 2004, Emotion.

[30]  Markus Junghöfer,et al.  Selective Visual Attention to Emotion , 2007, The Journal of Neuroscience.

[31]  R. Compton The interface between emotion and attention: a review of evidence from psychology and neuroscience. , 2003, Behavioral and cognitive neuroscience reviews.

[32]  Peter J. Lang,et al.  Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance , 2005, NeuroImage.

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

[34]  Johanna Kissler,et al.  People matter: Perceived sender identity modulates cerebral processing of socio-emotional language feedback , 2016, NeuroImage.

[35]  M. Junghöfer,et al.  How ‘love’ and ‘hate’ differ from ‘sleep’: Using combined electro/magnetoencephalographic data to reveal the sources of early cortical responses to emotional words , 2014, Human brain mapping.

[36]  Evgeniy Gabrilovich,et al.  Computing Semantic Relatedness Using Wikipedia-based Explicit Semantic Analysis , 2007, IJCAI.

[37]  Paul Pauli,et al.  Don't look at me in anger! Enhanced processing of angry faces in anticipation of public speaking. , 2010, Psychophysiology.

[38]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

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

[40]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[41]  J. Kissler,et al.  Cerebral correlates of faking: evidence from a brief implicit association test on doping attitudes , 2015, Front. Behav. Neurosci..

[42]  Cornelia Herbert,et al.  Emotion, Etmnooi, or Emitoon? – Faster lexical access to emotional than to neutral words during reading , 2013, Biological Psychology.

[43]  M. Posner,et al.  The attention system of the human brain: 20 years after. , 2012, Annual review of neuroscience.

[44]  Evelyn C. Ferstl,et al.  The Anterior Frontomedian Cortex and Evaluative Judgment: An fMRI Study , 2002, NeuroImage.

[45]  Lynne Milgram,et al.  Top Down versus Bottom Up , 1999 .

[46]  D. Bub,et al.  The Neural Substrate for Concrete, Abstract, and Emotional Word Lexica A Positron Emission Tomography Study , 1997, Journal of Cognitive Neuroscience.

[47]  M. Corbetta,et al.  Top-Down Control of Human Visual Cortex by Frontal and Parietal Cortex in Anticipatory Visual Spatial Attention , 2008, The Journal of Neuroscience.

[48]  Sonja A. Kotz,et al.  Attentional orienting towards emotion: P2 and N400 ERP effects , 2011, Neuropsychologia.

[49]  J. Kissler,et al.  Perceived Communicative Context and Emotional Content Amplify Visual Word Processing in the Fusiform Gyrus , 2015, The Journal of Neuroscience.

[50]  Tobias Flaisch,et al.  Emotion and the processing of symbolic gestures: an event-related brain potential study. , 2011, Social cognitive and affective neuroscience.

[51]  Wolfgang Grodd,et al.  Amygdala activation during reading of emotional adjectives--an advantage for pleasant content. , 2009, Social cognitive and affective neuroscience.

[52]  Ramin Assadollahi,et al.  Emotional and semantic networks in visual word processing: insights from ERP studies. , 2006, Progress in brain research.

[53]  Harold Goodglass,et al.  Laterality and sex differences for visual recognition of emotional and non-emotional words , 1981, Neuropsychologia.

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

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

[56]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[57]  Sara C. Sereno,et al.  Early emotion word processing: Evidence from event-related potentials , 2009, Biological Psychology.

[58]  Bruce W. Smith,et al.  The impact of affect and frequency on lexical decision: The role of the amygdala and inferior frontal cortex , 2006, NeuroImage.

[59]  Werner Sommer,et al.  P1 and beyond: functional separation of multiple emotion effects in word recognition. , 2012, Psychophysiology.

[60]  M. Bradley,et al.  Looking at pictures: affective, facial, visceral, and behavioral reactions. , 1993, Psychophysiology.

[61]  Thomas Straube,et al.  Brain activation during direct and indirect processing of positive and negative words , 2011, Behavioural Brain Research.

[62]  A. Jacobs,et al.  Affective processing within 1/10th of a second: High arousal is necessary for early facilitative processing of negative but not positive words , 2009, Cognitive, affective & behavioral neuroscience.

[63]  Kevin N. Ochsner,et al.  The neural correlates of direct and reflected self-knowledge , 2005, NeuroImage.

[64]  Vera Ferrari,et al.  Directed and Motivated Attention during Processing of Natural Scenes , 2008, Journal of Cognitive Neuroscience.

[65]  J. Kissler,et al.  Event related potentials to emotional adjectives during reading. , 2008, Psychophysiology.

[66]  W. Sommer,et al.  Time course and task dependence of emotion effects in word processing , 2009, Cognitive, affective & behavioral neuroscience.

[67]  Stephan Moratti,et al.  Prefrontal-Occipitoparietal Coupling Underlies Late Latency Human Neuronal Responses to Emotion , 2011, The Journal of Neuroscience.

[68]  W. Miltner,et al.  Brain activation to briefly presented emotional words: Effects of stimulus awareness , 2015, Human brain mapping.

[69]  M. Bradley,et al.  Emotional perception: correlation of functional MRI and event-related potentials. , 2006, Cerebral cortex.

[70]  Harald T. Schupp,et al.  Emotional Facilitation of Sensory Processing in the Visual Cortex , 2003, Psychological science.

[71]  J. Kissler,et al.  Buzzwords , 2007, Psychological science.

[72]  L. Pessoa How do emotion and motivation direct executive control? , 2009, Trends in Cognitive Sciences.

[73]  Allen Azizian,et al.  Beware misleading cues: perceptual similarity modulates the N2/P3 complex. , 2006, Psychophysiology.

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