Emotion–Perception Interplay in the Visual Cortex: “The Eyes Follow the Heart”

Emotive aspects of stimuli have been shown to modulate perceptual thresholds. Lately, studies using functional Magnetic Resonance Imaging (fMRI) showed that emotive aspects of visual stimuli activated not only canonical limbic regions, but also sensory areas in the cerebral cortex. However, it is still arguable to what extent such emotive, related activation in sensory areas of the cortex are affected by physical characteristic or attribute difference of stimuli. To manipulate valence of stimuli while keeping visual features largely unchanged, we took advantage of the Expressional Transfiguration (ET) of faces. In addition, to explore the sensitivity of high level visual regions, we compared repeated with unrepeated (i.e. different) stimuli presentations (fMR adaptation). Thus, the dynamics of brain responses was determined according to the relative signal reduction during “repeated” relative to “different” presentations (“adaptation ratio”). Our results showed, for the first time, that emotional valence produced significant differences in fMR adaptation, but not in overall levels of activation of lateral occipital complex (LOC). We then asked whether this emotion modulation on sensory cortex could be related to previous personal experience that attached negative attributes of stimuli. To clarify this, we investigated Posttraumatic Stress Disorder (PTSD) and non-PTSD veterans. PTSD is characterized by recurrent revival of trauma-related sensations. Such phenomena have been attributed to a disturbed processing of trauma-related stimuli, either at the perceptual level or at the cognitive level. We assumed that PTSD veterans would differ from non-PTSD veterans (who have similar combat experience) in their high order visual cortex responses to combat-related visual stimuli that are associated with their traumatic experience. An fMRI study measured the cerebral activation of subjects while viewing pictures with and without combat content, in “repeated” or “different” presentation conditions. The emotive effect on the visual cortex was found, again, only in the fMR-adaptation paradigm. Visual cortical regions showed significant differences between PTSD and non-PTSD veterans only in “repeated” presentations of trauma-related stimuli (i.e. combat). In these regions, PTSD veterans showed less decrease in signal with repeated presentations of the same combat-related stimuli. This finding points to the possibility that traumatic experience modulates brain activity at the level of sensory cortex itself.

[1]  Joseph E LeDoux The emotional brain , 1996 .

[2]  T. Hendler,et al.  A hierarchical axis of object processing stages in the human visual cortex. , 2001, Cerebral cortex.

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

[4]  Andrew W. Young,et al.  The enigma of the amygdala: on its contribution to human emotion , 2000 .

[5]  A. Young,et al.  Face processing impairments after amygdalotomy. , 1997, Brain : a journal of neurology.

[6]  A. Damasio,et al.  Non-conscious face recognition in patients with face agnosia , 1988, Behavioural Brain Research.

[7]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[8]  Peter J. Lang,et al.  Processing emotional pictures: Differential activation in primary visual cortex , 1996, NeuroImage.

[9]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[10]  Deborah J. Hellawell,et al.  Facial expression processing after amygdalotomy , 1996, Neuropsychologia.

[11]  Christian Grillon,et al.  Abnormal mismatch negativity in women with sexual assault-related posttraumatic stress disorder , 1999, Biological Psychiatry.

[12]  S. Taylor,et al.  The effect of graded aversive stimuli on limbic and visual activation , 2000, Neuropsychologia.

[13]  R. Bauer,et al.  Autonomic recognition of names and faces in prosopagnosia: A neuropsychological application of the guilty knowledge test , 1984, Neuropsychologia.

[14]  Joseph E LeDoux The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1996 .

[15]  J. S. Morris,et al.  The functional anatomy of innate and acquired fear: Perspectives from neuroimaging , 2000 .

[16]  Karl J. Friston,et al.  Brain Systems Mediating Aversive Conditioning: an Event-Related fMRI Study , 1998, Neuron.

[17]  N. Kanwisher Domain specificity in face perception , 2000, Nature Neuroscience.

[18]  Ralph Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  K. Grill-Spector,et al.  The dynamics of object-selective activation correlate with recognition performance in humans , 2000, Nature Neuroscience.

[20]  Kenji Kawano,et al.  Global and fine information coded by single neurons in the temporal visual cortex , 1999, Nature.

[21]  P. Lang The emotion probe. Studies of motivation and attention. , 1995, The American psychologist.

[22]  W. Singer,et al.  The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery , 1998, The European journal of neuroscience.

[23]  M. Bradley,et al.  Neuroanatomical correlates of pleasant and unpleasant emotion , 1997, Neuropsychologia.

[24]  R. McNally,et al.  Implicit and explicit memory bias for threat in post-traumatic stress disorder. , 1991, Behaviour research and therapy.

[25]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[26]  S. Edelman,et al.  Cue-Invariant Activation in Object-Related Areas of the Human Occipital Lobe , 1998, Neuron.

[27]  A. Bleich,et al.  Classification of Veterans with Post-Traumatic Stress Disorder Using Visual Brain Evoked P3s to Traumatic Stimuli , 1996, British Journal of Psychiatry.

[28]  P. Thompson,et al.  Margaret Thatcher: A New Illusion , 1980, Perception.

[29]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[30]  L Weiskrantz,et al.  Non-conscious recognition of affect in the absence of striate cortex. , 1999, Neuroreport.

[31]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

[32]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

[33]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Karl J. Friston,et al.  Brain systems mediating aversive conditioning: An event related fMRI study , 1998, NeuroImage.

[35]  Robert L. Morris,et al.  The relationships among performance on a prototype indicator of perceptual defence/vigilance, personality, and extrasensory perception , 1995 .

[36]  Joseph E LeDoux,et al.  Impaired fear conditioning following unilateral temporal lobectomy in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  N. Alpert,et al.  A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery. , 1996, Archives of general psychiatry.

[38]  H. Critchley,et al.  Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study , 2000, Human brain mapping.

[39]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[40]  T. Dalgleish,et al.  Information processing in post-traumatic stress disorder. , 1994, Behaviour research and therapy.

[41]  D. Broadbent,et al.  Perception of Emotionally Toned Words , 1967, Nature.

[42]  D. Jacobowitz,et al.  Serotonergic innervation of the forebrain: Effect of lesions on serotonin and tryptophan hydroxylase levels , 1977, Brain Research.

[43]  S. Taylor,et al.  The Effect of Emotional Content on Visual Recognition Memory: A PET Activation Study , 1998, NeuroImage.

[44]  L. Nadel,et al.  Cognitive neuroscience of emotion , 2000 .

[45]  Michael Davis,et al.  The role of the amygdala in fear and anxiety. , 1992, Annual review of neuroscience.

[46]  A. Ohman,et al.  Habituation of the electrodermal orienting reaction to potentially phobic and supposedly neutral stimuli in normal human subjects. , 1974, Biological psychology.

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

[48]  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 .

[49]  S. Edelman,et al.  Human Brain Mapping 6:316–328(1998) � A Sequence of Object-Processing Stages Revealed by fMRI in the Human Occipital Lobe , 2022 .

[50]  David G. Amaral,et al.  The role of the amygdala in primate social cognition. , 2000 .

[51]  A. Dale,et al.  New images from human visual cortex , 1996, Trends in Neurosciences.

[52]  S. Kosslyn,et al.  Neural effects of visualizing and perceiving aversive stimuli: a PET investigation. , 1996, Neuroreport.

[53]  Alex Martin,et al.  Properties and mechanisms of perceptual priming , 1998, Current Opinion in Neurobiology.

[54]  W. Singer,et al.  Functional imaging of mirror and inverse reading reveals separate coactivated networks for oculomotion and spatial transformations , 1998, Neuroreport.

[55]  J. Douglas Bremner,et al.  Does stress damage the brain? , 1999, Biological Psychiatry.

[56]  A. Young,et al.  Face perception after brain injury. Selective impairments affecting identity and expression. , 1993, Brain : a journal of neurology.

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

[58]  Edmund T. Rolls,et al.  Functions of the Primate Temporal Lobe Cortical Visual Areas in Invariant Visual Object and Face Recognition , 2000, Neuron.

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

[60]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

[61]  A. Calder Facial Emotion Recognition after Bilateral Amygdala Damage: Differentially Severe Impairment of Fear , 1996 .

[62]  R. Haley,et al.  Brain abnormalities in Gulf War syndrome: evaluation with 1H MR spectroscopy. , 2000, Radiology.

[63]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  H. Critchley,et al.  Neural Activity Relating to Generation and Representation of Galvanic Skin Conductance Responses: A Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[65]  C. Nemeroff,et al.  Neurobiology of posttraumatic stress disorder , 2000, Current Opinion in Neurobiology.

[66]  Joseph E. LeDoux,et al.  Cognitive–emotional interactions: Listen to the brain. , 2000 .

[67]  A. Bleich,et al.  Effect of repeated visual traumatic stimuli on the event related P3 brain potential in post-traumatic stress disorder. , 1996, The International journal of neuroscience.

[68]  E. T. Rolls,et al.  Activity of neurones in the inferotemporal cortex of the alert monkey , 1977, Brain Research.

[69]  Leslie G. Ungerleider,et al.  Complementary neural mechanisms for tracking items in human working memory. , 2000, Science.

[70]  R. Adolphs Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1997 .

[71]  T. Hendler,et al.  Feeling or Features Different Sensitivity to Emotion in High-Order Visual Cortex and Amygdala , 2001, Neuron.

[72]  M. Shepherd International Perspectives on DSM-III: Diagnostic and Statistical Manual of Mental Disorders: 3rd edn , 1984 .

[73]  R. Adolphs,et al.  Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans , 1995, Science.

[74]  P. Niedenthal,et al.  The heart's eye: Emotional influences in perception and attention. , 1994 .

[75]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

[76]  B. Horwitz,et al.  Brain activity during transient sadness and happiness in healthy women. , 1995, The American journal of psychiatry.

[77]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[78]  R. Dolan,et al.  Common effects of emotional valence, arousal and attention on neural activation during visual processing of pictures , 1999, Neuropsychologia.

[79]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[80]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

[81]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.