Temporal precedence of emotion over attention modulations in the lateral amygdala: Intracranial ERP evidence from a patient with temporal lobe epilepsy

Previous fMRI studies have reported mixed evidence for the influence of selective attention on amygdala responses to emotional stimuli, with some studies showing “automatic” emotional effects to threat-related stimuli without attention (or even without awareness), but other studies showing a gating of amygdala activity by selective attention with no response to unattended stimuli. We recorded intracranial local field potentials from the intact left lateral amygdala in a human patient prior to surgery for epilepsy and tested, with a millisecond time resolution, for neural responses to fearful faces appearing at either task-relevant or task-irrelevant locations. Our results revealed an early emotional effect in the amygdala arising prior to, and independently of, attentional modulation. However, at a later latency, we found a significant modulation of the differential emotional response when attention was directed toward or away from fearful faces. These results suggest separate influences of emotion and attention on amygdala activation and may help reconcile previous discrepancies concerning the relative responsiveness of the human amygdala to emotional and attentional factors.

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

[2]  D. Zald The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[3]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

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

[5]  Patrik Vuilleumier,et al.  Cholinergic enhancement modulates neural correlates of selective attention and emotional processing , 2003, NeuroImage.

[6]  A. Anderson,et al.  Neural Correlates of the Automatic Processing of Threat Facial Signals , 2022 .

[7]  Sheng He,et al.  Cortical Responses to Invisible Faces: Dissociating Subsystems for Facial-Information Processing , 2006, Current Biology.

[8]  O. Blanke,et al.  Intracranial Neurophysiological Correlates Related to the Processing of Faces , 2001, Epilepsy & Behavior.

[9]  Thomas M. Moerland,et al.  Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation , 2005, NeuroImage.

[10]  Geert Crombez,et al.  Mood-congruent attentional bias in dysphoria: maintained attention to and impaired disengagement from negative information. , 2005, Emotion.

[11]  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.

[12]  E. Halgren,et al.  Spatio-temporal stages in face and word processing. I. Depth-recorded potentials in the human occipital, temporal and parietal lobes [corrected]. , 1994, Journal of physiology, Paris.

[13]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  E. Phelps Emotion and cognition: insights from studies of the human amygdala. , 2006, Annual review of psychology.

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

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

[17]  Charles L. Wilson,et al.  Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects , 1997, Neuron.

[18]  W. Drevets Neuroimaging Abnormalities in the Amygdala in Mood Disorders , 2003, Annals of the New York Academy of Sciences.

[19]  R. Dolan,et al.  Amygdala Automaticity in Emotional Processing , 2003, Annals of the New York Academy of Sciences.

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

[21]  Nikos K. Logothetis,et al.  Facial-Expression and Gaze-Selective Responses in the Monkey Amygdala , 2007, Current Biology.

[22]  M. Mesulam,et al.  Selectively distributed processing of visual object recognition in the temporal and frontal lobes of the human brain , 1995, Annals of neurology.

[23]  A. Mikami,et al.  Activity of single neurons in the monkey amygdala during performance of a visual discrimination task. , 1992, Journal of neurophysiology.

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

[25]  Steven C.R. Williams,et al.  Time courses of left and right amygdalar responses to fearful facial expressions , 2001, NeuroImage.

[26]  C. Koch,et al.  Category-specific visual responses of single neurons in the human medial temporal lobe , 2000, Nature Neuroscience.

[27]  E. Halgren,et al.  Spatio-temporal stages in face and word processing. 1. Depth recorded potentials in the human occipital and parietal lobes , 1994, Journal of Physiology-Paris.

[28]  A. Anderson Affective influences on the attentional dynamics supporting awareness. , 2005, Journal of experimental psychology. General.

[29]  J. Gentle,et al.  Randomization and Monte Carlo Methods in Biology. , 1990 .

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

[31]  François Mauguière,et al.  Early Amygdala Reaction to Fear Spreading in Occipital, Temporal, and Frontal Cortex A Depth Electrode ERP Study in Human , 2004, Neuron.

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

[33]  K. Huhman,et al.  The Amygdala in Brain Function: Basic and Clinical Approaches Shinnick-Gallagher P , 2004, The Lancet Neurology.

[34]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

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

[36]  J. Driver,et al.  Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  T. Allison,et al.  Face recognition in human extrastriate cortex. , 1994, Journal of neurophysiology.

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

[39]  R. Adolphs,et al.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1994, Nature.

[40]  Gilles Pourtois,et al.  Dynamics of emotional effects on spatial attention in the human visual cortex. , 2006, Progress in brain research.

[41]  S. Paradiso The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[42]  E. Rolls,et al.  Neurons in the amygdala of the monkey with responses selective for faces , 1985, Behavioural Brain Research.

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

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

[45]  W. Drevets Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression. , 2000, Progress in brain research.

[46]  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.

[47]  M. Peelen,et al.  Direct intracranial recording of body-selective responses in human extrastriate visual cortex , 2007, Neuropsychologia.

[48]  Andreas Keil,et al.  Additive effects of emotional content and spatial selective attention on electrocortical facilitation. , 2005, Cerebral cortex.

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

[50]  Jeffrey S. Maxwell,et al.  Human Amygdala Responsivity to Masked Fearful Eye Whites , 2004, Science.

[51]  R. Dolan,et al.  Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study , 2002, Neuropsychologia.

[52]  Jason B. Mattingley,et al.  Differential amygdala responses to happy and fearful facial expressions depend on selective attention , 2005, NeuroImage.

[53]  S. Dehaene,et al.  A direct intracranial record of emotions evoked by subliminal words. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[55]  J. Eccles The actions of antidromic impulses on ganglion cells , 1936, The Journal of physiology.

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

[57]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[58]  G. Woodman,et al.  Event-related potential studies of attention , 2000, Trends in Cognitive Sciences.

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

[60]  Leslie G. Ungerleider,et al.  Attentional control of the processing of neural and emotional stimuli. , 2002, Brain research. Cognitive brain research.

[61]  John G. Taylor,et al.  Influence of attentional demands on the processing of emotional facial expressions in the amygdala , 2007, NeuroImage.

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

[63]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[64]  J. D. McGaugh,et al.  Role of the Basolateral Amygdala in Memory Consolidation , 2003, Annals of the New York Academy of Sciences.

[65]  Michael J. Brammer,et al.  A preferential increase in the extrastriate response to signals of danger , 2003, NeuroImage.

[66]  T. Allison,et al.  Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. , 1999, Cerebral cortex.

[67]  Brian N. Pasley,et al.  Subcortical Discrimination of Unperceived Objects during Binocular Rivalry , 2004, Neuron.

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

[69]  Patrik Vuilleumier,et al.  Beware and be aware: Capture of spatial attention by fear-related stimuli in neglect , 2001, Neuroreport.

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

[71]  D. Paré,et al.  A spatially structured network of inhibitory and excitatory connections directs impulse traffic within the lateral amygdala , 2006, Neuroscience.

[72]  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.

[73]  A. Young,et al.  Neuropsychology of fear and loathing , 2001 .

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

[75]  Alan Cowey,et al.  The neurobiology of blindsight , 1991, Trends in Neurosciences.

[76]  Luiz Pessoa,et al.  Target visibility and visual awareness modulate amygdala responses to fearful faces. , 2006, Cerebral cortex.