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Amygdala Damage Affects Event-Related Potentials for Fearful Faces at Specific Time Windows

By Pia Rotshtein, Mark P Richardson, Joel S Winston, Stefan J Kiebel, Patrik Vuilleumier, Martin Eimer, Jon Driver and Raymond J Dolan


The amygdala is known to influence processing of threat-related stimuli in distant brain regions, including visual cortex. The time-course of these distant influences is unknown, although this information is important for resolving debates over likely pathways mediating an apparent rapidity in emotional processing. To address this, we recorded event-related potentials (ERPs) to seen fearful face expressions, in preoperative patients with medial temporal lobe epilepsy who had varying degrees of amygdala pathology, plus healthy volunteers. We found that amygdala damage diminished ERPs for fearful versus neutral faces within the P1 time-range, ∼100–150 ms, and for a later component at ∼500–600 ms. Individual severity of amygdala damage determined the magnitude of both these effects, consistent with a causal amygdala role. By contrast, amygdala damage did not affect explicit perception of fearful expressions nor a distinct emotional ERP effect at 150–250 ms. These results demonstrate two distinct time-points at which the amygdala influences fear processing. The data also demonstrate that while not all aspects of expression processing are disrupted by amygdala damage, there is a crucial impact on an early P1 component. These findings are consistent with the existence of multiple processing stages or routes for fearful faces that vary in their dependence on amygdala function. Hum Brain Mapp, 2010. © 2009 Wiley-Liss, Inc

Topics: Research Article
Publisher: Wiley Subscription Services, Inc., A Wiley Company
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  1. (2005). A direct brainstem-amygdalacortical ‘alarm’ system for subliminal signals of fear.
  2. (1998). A neuromodulatory role for the human amygdala in processing emotional facial expressions.
  3. (1999). A subcortical pathway to the right amygdala mediating ‘‘unseen’’ fear.
  4. (2004). A temporal dissociation of subliminal versus supraliminal fear perception: An event-related potential study.
  5. (2005). Activity in the human brain predicting differential heart rate responses to emotional facial expressions.
  6. (2003). Amygdala automaticity in emotional processing.
  7. (2003). Amygdala damage impairs emotion recognition from scenes only when they contain facial expressions.
  8. (2005). Amygdala damage impairs emotional memory for gist but not details of complex stimuli.
  9. (2003). Amygdala, affect and cognition: Evidence from 10 patients with Urbach–Wiethe disease.
  10. (2005). Asymmetrical activation in the human brain during processing of fearful faces.
  11. (2002). Attentional control of the processing of neural and emotional stimuli.
  12. (1996). Brain events related to normal and moderately scrambled faces.
  13. (1996). Categorical perception of morphed facial expressions.
  14. (2005). Conjunction revisited.
  15. (2000). Contribution of the anteromedial temporal lobes to the evaluation of facial emotion.
  16. (2005). Contributions of the amygdala to emotion processing: From animal models to human behavior.
  17. (2002). Cortical sources of the early components of the visual evoked potential. Hum Brain Mapp 15:95–111.
  18. (1994). Damasio A
  19. (1998). Differential effects of amygdala lesions on early and late plastic components of auditory cortex spike trains during fear conditioning.
  20. (2007). Differential electrocortical responses to increasing intensities of fearful and happy emotional expressions.
  21. (2001). Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field.
  22. (2004). Differential neural responses to overt and covert presentations of facial expressions of fear and disgust.
  23. (2006). Differential stimuli and task effects in the amygdala and sensory areas.
  24. (2005). Discriminating emotional faces without primary visual cortices involves the right amygdala.
  25. (2004). Distant influences of amygdala lesion on visual cortical activation during emotional face processing.
  26. (2004). Early amygdala reaction to fear spreading in occipital, temporal, and frontal cortex: A depth electrode ERP study in human.
  27. (2001). Effects of attention and emotion on face processing in the human brain: An event-related fMRI study.
  28. (2001). Effects of emotional arousal in the cerebral hemispheres: A study of oscillatory brain activity and event-related potentials.
  29. (2004). Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cereb Cortex 14:619–633.
  30. (2002). Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli.
  31. (1996). Electrophysiological studies of face perception in humans.
  32. (2001). Emotion recognition from faces and prosody following temporal lobectomy.
  33. (2006). Emotional and semantic networks in visual word processing: Insights from ERP studies. Prog Brain Res 156:147–183.
  34. (1995). Emotional expression in upside-down faces: Evidence for configurational and componential processing.
  35. (2004). Emotional memory and perception in temporal lobectomy patients with amygdala damage.
  36. (2004). Encoding of emotional memories depends on amygdala and hippocampus and their interactions.
  37. (2006). Event related potentials and the perception of intensity in facial expressions.
  38. (2000). Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study.
  39. (2008). Express attentional re-engagement but delayed entry into consciousness following invalid spatial cues in visual search.
  40. (1998). Face processing impairments after encephalitis: Amygdala damage and recognition of fear.
  41. (1995). Fear and the human amygdala.
  42. (2000). Fear recognition deficits after focal brain damage: A cautionary note.
  43. (2001). Feeling or features: Different sensitivity to emotion in high-order visual cortex and amygdala.
  44. Friston KJ (2004a) Statistical parametric mapping for event-related potentials (II): A hierarchical temporal model.
  45. Friston KJ (2004b) Statistical parametric mapping for event-related potentials: I. Generic considerations.
  46. Friston KJ.2003. Random effects analysis.
  47. Holmes A (2002): An ERP study on the time course of emotional face processing.
  48. Holmes A (2007): Event-related brain potential correlates of emotional face processing.
  49. Holmes A (2008): Links between rapid ERP responses to fearful faces and conscious awareness.
  50. (2005). How brains beware: Neural mechanisms of emotional attention.
  51. (2000). Impaired emotional declarative memory following unilateral amygdala damage. Learn Mem 7:180–186.
  52. (2003). Impaired facial emotion recognition in early-onset right mesial temporal lobe epilepsy.
  53. (1995). Impaired fear conditioning following unilateral temporal lobectomy in humans.
  54. (2004). Impaired judgments of sadness but not happiness following bilateral amygdala damage.
  55. Ioannides A (2003): Time course of regional brain activations during facial emotion recognition in humans.
  56. (2001). Lesions of the human amygdala impair enhanced perception of emotionally salient events.
  57. Maravita A (2000): Electrophysiological correlates of conscious vision: Evidence from unilateral extinction.
  58. (2002). Measurement of amygdala T2 relaxation time in temporal lobe epilepsy.
  59. (2006). Memories for emotional autobiographical events following unilateral damage to medial temporal lobe.
  60. (2007). Neural responses to facial expression and face identity in the monkey amygdala.
  61. (1999). Nonconscious recognition of affect in the absence of striate cortex.
  62. (1999). Normal recognition of emotional similarity between facial expressions following bilateral amygdala damage.
  63. (2009). Occipital EEG correlates of conscious awareness when subjective target shine-through and effective visual masking are compared: Bifocal early increase in gamma power and speed-up of P1.
  64. (2004). Ohman A
  65. (2007). On the unconscious subcortical origin of human fear.
  66. Phelps EA (2000): Expression without recognition: Contributions of the human amygdala to emotional communication. Psychol Sci 11:106–111.
  67. (1976). Pictures of facial affect.
  68. (2002). r ERPs for Faces Following Amygdala Damage r r 1103 rDolan RJ
  69. r ERPs for Faces Following Amygdala Damage r r 1105 r
  70. r r 1104 rPessoa
  71. (2007). Rapid detection of fear in body expressions, an ERP study.
  72. (2003). Rapid extraction of emotional expression: Evidence from evoked potential fields during brief presentation of face stimuli.
  73. (2000). Recognition memory for emotionally negative and neutral words: An ERP study.
  74. (2007). Recognition of emotional face expressions and amygdala pathology.
  75. (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damage.
  76. (2006). Sequential ordering of morphed faces and facial expressions following temporal lobe damage.
  77. (2003). Source analysis of event-related cortical activity during visuo-spatial attention. Cereb Cortex 13:486–499.
  78. (1996). Speed of processing in the human visual system.
  79. (2002). Stages of processing in face perception.
  80. T (2005b) Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation.
  81. (2006). Task and content modulate amygdala-hippocampal connectivity in emotional retrieval.
  82. (2003). The amygdala, social behavior, and danger detection.
  83. (2004). The dynamics of cortico-amygdala and autonomic activity over the experimental time course of fear perception.
  84. (1996). The Emotional Brain.
  85. (1998). The human amygdala in social judgment.
  86. (2003). The interface between emotion and attention: A review of evidence from psychology and neuroscience.
  87. (2002). The primate amygdala and the neurobiology of social behavior: Implications for understanding social anxiety. Biol Psychiatry 51:11–17.
  88. (2003). The processing of emotional facial expression is gated by spatial attention: Evidence from event-related brain potentials.
  89. (2007). The role of attention and relatedness in emotionally enhanced memory.
  90. (2005). The role of the amygdala in human fear: Automatic detection of threat.
  91. (2004). Time course and specificity of event-related potentials to emotional expressions.
  92. Treese AC (2004): Recognition memory for emotional and neutral faces: An event-related potential study.
  93. (2005). Two electrophysiological stages of spatial orienting towards fearful faces: Early temporo-parietal activation preceding gain control in extrastriate visual cortex.
  94. (2005). Unconscious fear influences emotional awareness of faces and voices.
  95. (1999). Visual evoked potentials in humans during recognition of emotional facial expressions.
  96. Vuilleumier P (2005a) Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: Time course and topographic evoked-potentials mapping.