Cerebral Correlates of Emotional and Action Appraisals During Visual Processing of Emotional Scenes Depending on Spatial Frequency: A Pilot Study

Visual processing of emotional stimuli critically depends on the type of cognitive appraisal involved. The present fMRI pilot study aimed to investigate the cerebral correlates involved in the visual processing of emotional scenes in two tasks, one emotional, based on the appraisal of personal emotional experience, and the other motivational, based on the appraisal of the tendency to action. Given that the use of spatial frequency information is relatively flexible during the visual processing of emotional stimuli depending on the task’s demands, we also explored the effect of the type of spatial frequency in visual stimuli in each task by using emotional scenes filtered in low spatial frequency (LSF) and high spatial frequencies (HSF). Activation was observed in the visual areas of the fusiform gyrus for all emotional scenes in both tasks, and in the amygdala for unpleasant scenes only. The motivational task induced additional activation in frontal motor-related areas (e.g. premotor cortex, SMA) and parietal regions (e.g. superior and inferior parietal lobules). Parietal regions were recruited particularly during the motivational appraisal of approach in response to pleasant scenes. These frontal and parietal activations, respectively, suggest that motor and navigation processes play a specific role in the identification of the tendency to action in the motivational task. Furthermore, activity observed in the motivational task, in response to both pleasant and unpleasant scenes, was significantly greater for HSF than for LSF scenes, suggesting that the tendency to action is driven mainly by the detailed information contained in scenes. Results for the emotional task suggest that spatial frequencies play only a small role in the evaluation of unpleasant and pleasant emotions. Our preliminary study revealed a partial distinction between visual processing of emotional scenes during identification of the tendency to action, and during identification of personal emotional experiences. It also illustrates flexible use of the spatial frequencies contained in scenes depending on their emotional valence and on task demands.

[1]  L. Deecke,et al.  The Preparation and Execution of Self-Initiated and Externally-Triggered Movement: A Study of Event-Related fMRI , 2002, NeuroImage.

[2]  J. Grafman,et al.  The Human Amygdala: An Evolved System for Relevance Detection , 2003, Reviews in the neurosciences.

[3]  Florin Dolcos,et al.  Effects of aging on functional connectivity of the amygdala during negative evaluation: A network analysis of fMRI data , 2010, Neurobiology of Aging.

[4]  C. Carver,et al.  Anger is an approach-related affect: evidence and implications. , 2009, Psychological bulletin.

[5]  Dimitri Van De Ville,et al.  White-Matter Connectivity between Face-Responsive Regions in the Human Brain , 2012 .

[6]  Martial Mermillod,et al.  Coarse scales are sufficient for efficient categorization of emotional facial expressions: Evidence from neural computation , 2010, Neurocomputing.

[7]  Greg J Siegle,et al.  Common and distinct brain networks underlying explicit emotional evaluation: a meta-analytic study. , 2012, Social cognitive and affective neuroscience.

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

[9]  Kevin N. Ochsner,et al.  Attention and emotion: Does rating emotion alter neural responses to amusing and sad films? , 2005, NeuroImage.

[10]  B. Vogt Pain and emotion interactions in subregions of the cingulate gyrus , 2005, Nature Reviews Neuroscience.

[11]  Ralph Adolphs,et al.  Fear, faces, and the human amygdala , 2008, Current Opinion in Neurobiology.

[12]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[13]  E. Phelps Human emotion and memory: interactions of the amygdala and hippocampal complex , 2004, Current Opinion in Neurobiology.

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

[15]  Jean-Luc Anton,et al.  The role of human left superior parietal lobule in body part localization , 2004, Annals of neurology.

[16]  E. Halgren,et al.  Cognitive response profile of the human fusiform face area as determined by MEG. , 2000, Cerebral cortex.

[17]  D. Schacter,et al.  Processing emotional pictures and words: Effects of valence and arousal , 2006, Cognitive, affective & behavioral neuroscience.

[18]  Maureen McHugo,et al.  Enhanced Visual Cortical Activation for Emotional Stimuli is Preserved in Patients with Unilateral Amygdala Resection , 2013, The Journal of Neuroscience.

[19]  E. Fox,et al.  Facial Expressions of Emotion: Are Angry Faces Detected More Efficiently? , 2000, Cognition & emotion.

[20]  Swann Pichon,et al.  Threat prompts defensive brain responses independently of attentional control. , 2012, Cerebral cortex.

[21]  Martial Mermillod,et al.  Please Scroll down for Article Connection Science the Importance of Low Spatial Frequency Information for Recognising Fearful Facial Expressions the Importance of Low Spatial Frequency Information for Recognising Fearful Facial Expressions , 2022 .

[22]  B. Vogt,et al.  Structural and functional dichotomy of human midcingulate cortex , 2003, The European journal of neuroscience.

[23]  E. Rolls,et al.  The orbitofrontal cortex and beyond: From affect to decision-making , 2008, Progress in Neurobiology.

[24]  Stefan J. Kiebel,et al.  Amygdala damage affects event‐related potentials for fearful faces at specific time windows , 2009, Human brain mapping.

[25]  N. Frijda Emotion, cognitive structure and action tendency , 1987 .

[26]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

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

[28]  Parashkev Nachev,et al.  Space and the parietal cortex , 2007, Trends in Cognitive Sciences.

[29]  D. Amaral,et al.  Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey , 2003, Neuroscience.

[30]  J. Wilson,et al.  Circuitry of the dorsal lateral geniculate nucleus in the cat and monkey. , 1993, Acta anatomica.

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

[32]  R. Morecraft,et al.  Convergence of Limbic Input to the Cingulate Motor Cortex in the Rhesus Monkey , 1998, Brain Research Bulletin.

[33]  A. Oliva,et al.  Coarse Blobs or Fine Edges? Evidence That Information Diagnosticity Changes the Perception of Complex Visual Stimuli , 1997, Cognitive Psychology.

[34]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[35]  M. Bradley,et al.  Motivated attention: Affect, activation, and action. , 1997 .

[36]  P. Montoya,et al.  Low spatial frequency filtering modulates early brain processing of affective complex pictures , 2007, Neuropsychologia.

[37]  Jerzy Bodurka,et al.  Prefrontal Control of the Amygdala during Real-Time fMRI Neurofeedback Training of Emotion Regulation , 2013, PloS one.

[38]  Jürgen Kompenhans,et al.  Experimental methods for multi-diagnostics of flow fields in wind tunnels , 2007, J. Vis..

[39]  Dan Foti,et al.  Deconstructing Reappraisal: Descriptions Preceding Arousing Pictures Modulate the Subsequent Neural Response , 2008, Journal of Cognitive Neuroscience.

[40]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

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

[42]  J. Fagot,et al.  Categorizing facial identities, emotions, and genders: attention to high- and low-spatial frequencies by children and adults. , 2005, Journal of experimental child psychology.

[43]  G. Humphreys,et al.  Effects of spatial frequency bands on perceptual decision: it is not the stimuli but the comparison. , 2010, Journal of vision.

[44]  P. Jackson,et al.  The neural network of motor imagery: An ALE meta-analysis , 2013, Neuroscience & Biobehavioral Reviews.

[45]  GABAA receptors in the central nucleus of amygdala (CeA) affect on pain modulation , 2008, Brain Research.

[46]  Sandrine Delord,et al.  Which Mask is the Most Efficient: A Pattern or a Noise? It Depends on the Task , 1998 .

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

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

[49]  P. Bex,et al.  Spatial frequency, phase, and the contrast of natural images. , 2002, Journal of the Optical Society of America. A, Optics, image science, and vision.

[50]  Benjamin D. Lester,et al.  The Role of the Right Superior Parietal Lobule in Processing Visual Context for the Establishment of the Egocentric Reference Frame , 2014, Journal of Cognitive Neuroscience.

[51]  A. Oliva,et al.  Dr. Angry and Mr. Smile: when categorization flexibly modifies the perception of faces in rapid visual presentations , 1999, Cognition.

[52]  Greg Hajcak,et al.  Attending to affect: appraisal strategies modulate the electrocortical response to arousing pictures. , 2006, Emotion.

[53]  A. Keil,et al.  Modulation of the C1 visual event-related component by conditioned stimuli: evidence for sensory plasticity in early affective perception. , 2006, Cerebral cortex.

[54]  John J. B. Allen,et al.  Anger and frontal brain activity: EEG asymmetry consistent with approach motivation despite negative affective valence. , 1998, Journal of personality and social psychology.

[55]  Sara López-Martín,et al.  An electrophysiological study on the interaction between emotional content and spatial frequency of visual stimuli , 2007, Neuropsychologia.

[56]  Martin Lotze,et al.  The functional connectivity between amygdala and extrastriate visual cortex activity during emotional picture processing depends on stimulus novelty , 2011, Biological Psychology.

[57]  N. Hadjikhani,et al.  Fear fosters flight: a mechanism for fear contagion when perceiving emotion expressed by a whole body. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Anbupalam Thalamuthu,et al.  Genetics of Microstructure of the Corpus Callosum in Older Adults , 2014, PloS one.

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

[60]  Thomas J. Ross,et al.  Amygdala response to both positively and negatively valenced stimuli , 2001, Neuroreport.

[61]  D. Hassabis,et al.  From Threat to Fear: The Neural Organization of Defensive Fear Systems in Humans , 2009, The Journal of Neuroscience.

[62]  E. Harmon-Jones,et al.  The Effect of Personal Relevance and Approach-Related Action Expectation on Relative Left Frontal Cortical Activity , 2006, Psychological science.

[63]  D. Lundqvist,et al.  Karolinska Directed Emotional Faces , 2015 .

[64]  J. O'Doherty,et al.  Lights, Camembert, Action! The Role of Human Orbitofrontal Cortex in Encoding Stimuli, Rewards, and Choices , 2007, Annals of the New York Academy of Sciences.

[65]  D. Wolpert,et al.  Maintaining internal representations: the role of the human superior parietal lobe , 1998, Nature Neuroscience.

[66]  Simon J Graham,et al.  An fMRI study investigating cognitive modulation of brain regions associated with emotional processing of visual stimuli , 2003, Neuropsychologia.

[67]  Derek K. Jones,et al.  Occipito-temporal connections in the human brain. , 2003, Brain : a journal of neurology.

[68]  P. Fox,et al.  The role of anterior midcingulate cortex in cognitive motor control , 2014, Human brain mapping.

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

[70]  C. H. Hansen,et al.  Finding the face in the crowd: an anger superiority effect. , 1988, Journal of personality and social psychology.

[71]  R. Zeelenberg,et al.  Emotion-induced trade-offs in spatiotemporal vision. , 2011, Journal of experimental psychology. General.

[72]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

[73]  P. Vuilleumier,et al.  Effects of emotion regulation strategy on brain responses to the valence and social content of visual scenes , 2011, Neuropsychologia.

[74]  M. Eimer,et al.  The role of spatial frequency information for ERP components sensitive to faces and emotional facial expression. , 2005, Brain research. Cognitive brain research.

[75]  Heather L. Urry,et al.  Amygdala and Ventromedial Prefrontal Cortex Are Inversely Coupled during Regulation of Negative Affect and Predict the Diurnal Pattern of Cortisol Secretion among Older Adults , 2006, The Journal of Neuroscience.

[76]  Rudolf Stark,et al.  The embodied nature of motor imagery: the influence of posture and perspective , 2009, Experimental Brain Research.

[77]  K. Zilles,et al.  An investigation of the structural, connectional, and functional subspecialization in the human amygdala , 2012, Human brain mapping.

[78]  J. Stainer,et al.  The Emotions , 1882, Nature.

[79]  Martial Mermillod,et al.  Are Coarse Scales Sufficient for Fast Detection of Visual Threat? , 2010, Psychological science.

[80]  A. Anderson,et al.  Salience , State , and Expression : The Influence of Specific Aspects of Emotion on Attention and Perception , 2011 .

[81]  J. Baron,et al.  Does motor imagery share neural networks with executed movement: a multivariate fMRI analysis , 2013, Front. Hum. Neurosci..

[82]  E. Rolls,et al.  In linking affect to action: critical contributions of the orbitofrontal cortex , 2007 .

[83]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[84]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[85]  A. Campagne,et al.  Behavioral assessment of emotional and motivational appraisal during visual processing of emotional scenes depending on spatial frequencies , 2013, Brain and Cognition.

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

[87]  D. Hassabis,et al.  When Fear Is Near: Threat Imminence Elicits Prefrontal-Periaqueductal Gray Shifts in Humans , 2007, Science.

[88]  Daniel S. Margulies,et al.  Functional connectivity of the human amygdala using resting state fMRI , 2009, NeuroImage.

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

[90]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[91]  Jejo D. Koola,et al.  Emotion facilitates action: a transcranial magnetic stimulation study of motor cortex excitability during picture viewing. , 2007, Psychophysiology.

[92]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[93]  M. Bradley,et al.  Emotion and motivation I: defensive and appetitive reactions in picture processing. , 2001, Emotion.

[94]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[95]  Bradford C. Dickerson,et al.  Novelty as a dimension in the affective brain , 2010, NeuroImage.

[96]  T. Kimura,et al.  Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus , 2002, Neuroscience Letters.

[97]  M. Packard,et al.  Affective modulation of multiple memory systems , 2001, Current Opinion in Neurobiology.

[98]  Joseph E LeDoux,et al.  Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior , 2005, Neuron.

[99]  John D E Gabrieli,et al.  Bottom-Up and Top-Down Processes in Emotion Generation , 2009, Psychological science.

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

[101]  Anne Springer,et al.  Predicting and memorizing observed action: Differential premotor cortex involvement , 2011, Human brain mapping.

[102]  S. Yantis,et al.  Cortical mechanisms of space-based and object-based attentional control , 2003, Current Opinion in Neurobiology.

[103]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[104]  Peter J. Lang,et al.  Attention and Orienting : Sensory and Motivational Processes , 1997 .

[105]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

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

[107]  Justin S. Feinstein,et al.  The Human Amygdala and the Induction and Experience of Fear , 2011, Current Biology.

[108]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[109]  K. Mogg,et al.  Coarse threat images reveal theta oscillations in the amygdala: A magnetoencephalography study , 2009, Cognitive, affective & behavioral neuroscience.

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

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

[112]  Laurent Vercueil,et al.  Brain Processing of Emotional Scenes in Aging: Effect of Arousal and Affective Context , 2014, PloS one.

[113]  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.

[114]  R. Knight,et al.  PSYCHOLOGICAL SCIENCE Research Article Controlling the Integration of Emotion and Cognition The Role of Frontal Cortex in Distinguishing Helpful From Hurtful Emotional Information , 2022 .

[115]  H. Kornhuber,et al.  Distribution of readiness potential, pre-motion positivity, and motor potential of the human cerebral cortex preceding voluntary finger movements , 2004, Experimental Brain Research.

[116]  S. Kosslyn,et al.  The Oxford handbook of cognitive neuroscience , 2013 .

[117]  A. Sack Parietal cortex and spatial cognition , 2009, Behavioural Brain Research.

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

[119]  M. Bradley,et al.  Emotion and the motivational brain , 2010, Biological Psychology.

[120]  A. Holmes,et al.  The involvement of distinct visual channels in rapid attention towards fearful facial expressions , 2005 .

[121]  D. Weinberger,et al.  Neocortical modulation of the amygdala response to fearful stimuli , 2003, Biological Psychiatry.