Fearful faces impact in peripheral vision: Behavioral and neural evidence

Many studies provided evidence that the emotional content of visual stimulations modulates behavioral performance and neuronal activity. Surprisingly, these studies were carried out using stimulations presented in the center of the visual field while the majority of visual events firstly appear in the peripheral visual field. In this study, we assessed the impact of the emotional facial expression of fear when projected in near and far periphery. Sixteen participants were asked to categorize fearful and neutral faces projected at four peripheral visual locations (15° and 30° of eccentricity in right and left sides of the visual field) while reaction times and event-related potentials (ERPs) were recorded. ERPs were analyzed by means of spatio-temporal principal component and baseline-to-peak methods. Behavioral data confirmed the decrease of performance with eccentricity and showed that fearful faces induced shorter reaction times than neutral ones. Electrophysiological data revealed that the spatial position and the emotional content of faces modulated ERPs components. In particular, the amplitude of N170 was enhanced by fearful facial expression. These findings shed light on how visual eccentricity modulates the processing of emotional faces and suggest that, despite impoverished visual conditions, the preferential neural coding of fearful expression of faces still persists in far peripheral vision. The emotional content of faces could therefore contribute to their foveal or attentional capture, like in social interactions.

[1]  Martin Eimer,et al.  Attentional capture by task-irrelevant fearful faces is revealed by the N2pc component , 2007, Biological Psychology.

[2]  S. Mineka,et al.  Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. , 2001, Psychological review.

[3]  Jyrki Rovamo,et al.  Identification of facial images in peripheral vision , 2001, Vision Research.

[4]  R. Anderson,et al.  Aliasing in peripheral vision for counterphase gratings. , 1996, Journal of the Optical Society of America. A, Optics, image science, and vision.

[5]  Dominique Lamy,et al.  Attentional bias in anxiety: A behavioral and ERP study , 2005, Brain and Cognition.

[6]  C. Darwin The Expression of the Emotions in Man and Animals , .

[7]  Edward T. Bullmore,et al.  Differential neural responses to overt and covert presentations of facial expressions of fear and disgust , 2000, NeuroImage.

[8]  M. Eimer,et al.  Event-related brain potential correlates of emotional face processing , 2007, Neuropsychologia.

[9]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[10]  Yasuhiko Saito,et al.  An ERP investigation of emotional processing in European and Japanese individuals , 2006, Brain Research.

[11]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[12]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

[13]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  S. Liversedge,et al.  Saccadic eye movements and cognition , 2000, Trends in Cognitive Sciences.

[15]  Maurizio Codispoti,et al.  Peripheral vision and preferential emotion processing , 2009, Neuroreport.

[16]  R. Masland Neuronal cell types , 2004, Current Biology.

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

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

[19]  J. Davidoff,et al.  Brain events related to normal and moderately scrambled faces. , 1996, Brain research. Cognitive brain research.

[20]  P Vuilleumier,et al.  Neural response to emotional faces with and without awareness: event-related fMRI in a parietal patient with visual extinction and spatial neglect , 2002, Neuropsychologia.

[21]  R. Shapley,et al.  Background light and the contrast gain of primate P and M retinal ganglion cells. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M Mackeben,et al.  The importance of sustained attention for patients with maculopathies , 2000, Vision Research.

[23]  C. Tenke,et al.  Optimizing PCA methodology for ERP component identification and measurement: theoretical rationale and empirical evaluation , 2003, Clinical Neurophysiology.

[24]  L. Nummenmaa,et al.  Enhanced Processing of Emotional Gist in Peripheral Vision , 2009, The Spanish journal of psychology.

[25]  P Krolak-Salmon,et al.  Processing of facial emotional expression: spatio‐temporal data as assessed by scalp event‐related potentials , 2001, The European journal of neuroscience.

[26]  C. Curcio,et al.  Topography of ganglion cells in human retina , 1990, The Journal of comparative neurology.

[27]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[28]  W. Sato,et al.  Right hemispheric dominance in processing of unconscious negative emotion , 2006, Brain and Cognition.

[29]  A. Flykt,et al.  Emotion drives attention: detecting the snake in the grass. , 2001 .

[30]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

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

[32]  Joel Pokorny,et al.  Rod inputs to macaque ganglion cells , 1997, Vision Research.

[33]  Sakiko Yoshikawa,et al.  Emotional expression boosts early visual processing of the face: ERP recording and its decomposition by independent component analysis , 2001, Neuroreport.

[34]  Andreas J Fallgatter,et al.  Face-specific event-related potential in humans is independent from facial expression. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  G. Alpers,et al.  Here is looking at you: emotional faces predominate in binocular rivalry. , 2007, Emotion.

[36]  Dimitri J. Bayle,et al.  Unconsciously Perceived Fear in Peripheral Vision Alerts the Limbic System: A MEG Study , 2009, PloS one.

[37]  Dietrich Lehmann,et al.  Affective judgments of faces modulate early activity (approximately 160 ms) within the fusiform gyri. , 2002, NeuroImage.

[38]  Patrik Vuilleumier,et al.  Time course and specificity of event-related potentials to emotional expressions , 2004, Neuroreport.

[39]  Simon Rigoulot,et al.  Arousal and valence effects on event-related P3a and P3b during emotional categorization. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[40]  Tony W Buchanan,et al.  Retrieval of emotional memories. , 2007, Psychological bulletin.

[41]  E. Donchin,et al.  Spatiotemporal analysis of the late ERP responses to deviant stimuli. , 2001, Psychophysiology.

[42]  N. Kanwisher,et al.  A Preference for Contralateral Stimuli in Human Object- and Face-Selective Cortex , 2007, PloS one.

[43]  Arne Öhman,et al.  On the automatic nature of phobic fear: conditioned electrodermal responses to masked fear-relevant stimuli. , 1993, Journal of abnormal psychology.

[44]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[45]  R. Masland The fundamental plan of the retina , 2001, Nature Neuroscience.

[46]  R. Näsänen,et al.  Recognition of band-pass filtered hand-written numerals in foveal and peripheral vision , 1998, Vision Research.

[47]  R. Dolan,et al.  Distinct spatial frequency sensitivities for processing faces and emotional expressions , 2003, Nature Neuroscience.

[48]  G. Kerkhoff,et al.  Neurovisual rehabilitation: recent developments and future directions , 2000, American journal of ophthalmology.

[49]  A. Ohman,et al.  On the automatic nature of phobic fear: conditioned electrodermal responses to masked fear-relevant stimuli. , 1993, Journal of abnormal psychology.

[50]  D. Grandjean,et al.  Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: Time course and topographic evoked‐potentials mapping , 2005, Human brain mapping.

[51]  Ralph Adolphs,et al.  Processing of the Arousal of Subliminal and Supraliminal Emotional Stimuli by the Human Amygdala , 2003, The Journal of Neuroscience.

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

[53]  Muriel Boucart,et al.  Colour recognition at large visual eccentricities in normal observers and patients with low vision , 2006, Neuroreport.

[54]  K. Rayner Eye movements in reading and information processing: 20 years of research. , 1998, Psychological bulletin.

[55]  S. Delplanque,et al.  Event-related P3a and P3b in response to unpredictable emotional stimuli , 2005, Biological Psychology.

[56]  U. Grünert Anatomical Evidence for Rod Input to the Parvocellular Pathway in the Visual System of the Primate , 1997, The European journal of neuroscience.

[57]  L. Brothers,et al.  Response of neurons in the macaque amygdala to complex social stimuli , 1990, Behavioural Brain Research.

[58]  E. Fox Processing emotional facial expressions: The role of anxiety and awareness , 2002, Cognitive, affective & behavioral neuroscience.

[59]  A. L. I︠A︡rbus Eye Movements and Vision , 1967 .

[60]  F. Lepore,et al.  Women process multisensory emotion expressions more efficiently than men , 2010, Neuropsychologia.

[61]  F. McGlone,et al.  The role of spatial attention in the processing of facial expression: An ERP study of rapid brain responses to six basic emotions , 2003, Cognitive, affective & behavioral neuroscience.

[62]  H H Bülthoff,et al.  Detection of animals in natural images using far peripheral vision , 2001, The European journal of neuroscience.

[63]  Andreas A. Ioannides,et al.  Emotion Separation Is Completed Early and It Depends on Visual Field Presentation , 2010, PloS one.

[64]  L. Weiskrantz,et al.  Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. , 2001, Brain : a journal of neurology.

[65]  Chantal Kemner,et al.  Is the early modulation of brain activity by fearful facial expressions primarily mediated by coarse low spatial frequency information? , 2009, Journal of vision.

[66]  Hideko F. Norman,et al.  Aging and the cross modal perception of natural object shape , 2005 .

[67]  A. Young,et al.  Recognition of facial emotion in nine individuals with bilateral amygdala damage , 1999, Neuropsychologia.

[68]  J. Borod,et al.  Interhemispheric and intrahemispheric control of emotion: a focus on unilateral brain damage. , 1992, Journal of consulting and clinical psychology.

[69]  R. Larsen,et al.  Affect intensity as an individual difference characteristic: A review , 1987 .

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

[71]  Jeff T. Larsen,et al.  May I have your attention, please: Electrocortical responses to positive and negative stimuli , 2003, Neuropsychologia.

[72]  Margot J. Taylor,et al.  Source analysis of the N170 to faces and objects , 2004, Neuroreport.

[73]  Adam P. Morris,et al.  Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression , 2004, The Journal of Neuroscience.

[74]  R. Zeelenberg,et al.  Emotion Improves and Impairs Early Vision , 2009, Psychological science.

[75]  M. Eimer,et al.  An ERP study on the time course of emotional face processing , 2002, Neuroreport.

[76]  E. Donchin,et al.  A componential analysis of the ERP elicited by novel events using a dense electrode array. , 1999, Psychophysiology.

[77]  J. Stephen,et al.  Central versus peripheral visual field stimulation results in timing differences in dorsal stream sources as measured with MEG , 2002, Vision Research.

[78]  E. Rossi,et al.  The relationship between visual resolution and cone spacing in the human fovea , 2009, Nature Neuroscience.

[79]  Margot J. Taylor,et al.  Early processing of the six basic facial emotional expressions. , 2003, Brain research. Cognitive brain research.

[80]  S. Delplanque,et al.  Beyond Conventional Event-related Brain Potential (ERP): Exploring the Time-course of Visual Emotion Processing Using Topographic and Principal Component Analyses , 2008, Brain Topography.

[81]  G. Crombez,et al.  Pain demands attention: a cognitive-affective model of the interruptive function of pain. , 1999, Psychological bulletin.

[82]  M Esslen,et al.  Brain areas and time course of emotional processing , 2004, NeuroImage.

[83]  S. Delplanque,et al.  Modulation of cognitive processing by emotional valence studied through event-related potentials in humans , 2004, Neuroscience Letters.

[84]  Leanne M Williams,et al.  Amygdala–prefrontal dissociation of subliminal and supraliminal fear , 2006, Human brain mapping.

[85]  Paul Pauli,et al.  Binocular rivalry between emotional and neutral stimuli: a validation using fear conditioning and EEG. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[86]  Karine Sergerie,et al.  The role of the amygdala in emotional processing: A quantitative meta-analysis of functional neuroimaging studies , 2008, Neuroscience & Biobehavioral Reviews.

[87]  J. Tanaka,et al.  The NimStim set of facial expressions: Judgments from untrained research participants , 2009, Psychiatry Research.

[88]  S Zeki,et al.  A direct projection from area V1 to area V3A of rhesus monkey visual cortex , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[89]  M. Junghöfer,et al.  Attention and emotion: an ERP analysis of facilitated emotional stimulus processing , 2003, Neuroreport.

[90]  A. Jedynak,et al.  Rapid extraction of emotional expression: evidence from evoked potential fields during brief presentation of face stimuli , 2003, Neuropsychologia.

[91]  Barry B. Lee,et al.  Mesopic spectral responses and the purkinje shift of macaque lateral geniculate nucleus cells , 1987, Vision Research.

[92]  R Bruyer,et al.  Human gender differences in an emotional visual oddball task: an event-related potentials study , 2004, Neuroscience Letters.

[93]  Faraz Farzin,et al.  Dynamic Object Representations in Infants with and without Fragile X Syndrome , 2009, Front. Hum. Neurosci..

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

[95]  R. Adolphs Cognitive neuroscience: Cognitive neuroscience of human social behaviour , 2003, Nature Reviews Neuroscience.

[96]  Dietrich Lehmann,et al.  Affective Judgments of Faces Modulate Early Activity (∼160 ms) within the Fusiform Gyri , 2002, NeuroImage.

[97]  A. Kring,et al.  Sex differences in emotion: expression, experience, and physiology. , 1998, Journal of personality and social psychology.

[98]  Francesco Versace,et al.  Affective picture perception: Emotion, context, and the late positive potential , 2008, Brain Research.

[99]  J. Honoré,et al.  Human Neuroscience , 2022 .

[100]  Simon Rigoulot,et al.  Peripherally Presented Emotional Scenes: A Spatiotemporal Analysis of Early ERP Responses , 2008, Brain Topography.

[101]  D. Lehmann,et al.  Rapid emotional face processing in the human right and left brain hemispheres: an ERP study. , 1999, Neuroreport.

[102]  A. Mathews,et al.  A Cognitive Model of Selective Processing in Anxiety , 1998, Cognitive Therapy and Research.

[103]  B. Boycott,et al.  Retinal ganglion cell density and cortical magnification factor in the primate , 1990, Vision Research.

[104]  P. Lang,et al.  Parafoveal semantic processing of emotional visual scenes. , 2005, Journal of experimental psychology. Human perception and performance.

[105]  Wenfeng Feng,et al.  Three stages of facial expression processing: ERP study with rapid serial visual presentation , 2010, NeuroImage.

[106]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[107]  M. G. Calvo,et al.  Affective priming of emotional pictures in parafoveal vision: Left visual field advantage , 2008, Cognitive, affective & behavioral neuroscience.

[108]  M. Bradley,et al.  Emotion and motivation II: sex differences in picture processing. , 2001, Emotion.

[109]  Muriel Boucart,et al.  Face or building superiority in peripheral vision reversed by task requirements , 2009, Advances in cognitive psychology.

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

[111]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

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

[113]  Gordon E. Legge,et al.  Psychophysics of reading. XVIII. The effect of print size on reading speed in normal peripheral vision , 1998, Vision Research.

[114]  Manuel G. Calvo,et al.  Processing of emotional visual scenes outside the focus of spatial attention: The role of eccentricity , 2006 .

[115]  L. Obler,et al.  Right hemisphere emotional perception: evidence across multiple channels. , 1998, Neuropsychology.

[116]  D. Grandjean,et al.  Electrophysiological correlates of rapid spatial orienting towards fearful faces. , 2004, Cerebral cortex.

[117]  M. Eimer,et al.  ERPs reveal subliminal processing of fearful faces. , 2008, Psychophysiology.

[118]  Jesse S. Husk,et al.  Spatial scaling factors explain eccentricity effects on face ERPs. , 2005, Journal of vision.