Rapid amygdala gamma oscillations in response to fearful facial expressions

Neuropsychologia

Volumn 49, Issue 4, 2011, Pages 612-617

  Sato, Wataru ^a   Kochiyama, Takanori ^b   Uono, Shota ^a   Matsuda, Kazumi ^c   Usui, Keiko ^c   Inoue, Yushi ^c   Toichi, Motomi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b ADVANCED TELECOMMUNICATIONS RESEARCH INSTITUTE INTERNATIONAL   (Japan)

^c SHIZUOKA INSTITUTE OF EPILEPSY AND NEUROLOGICAL DISORDERS   (Japan)

Author keywords

Amygdala; Emotional facial expression; Gamma oscillation; Intracranial field potential recording

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN MAPPING; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRIC POTENTIAL; FACIAL EXPRESSION; FEAR; FEMALE; GAMMA RHYTHM; HUMAN; MALE; NEUROIMAGING; OSCILLATION; PATTERN RECOGNITION; PERCEPTIVE DISCRIMINATION; STIMULUS RESPONSE; TASK PERFORMANCE; TIME; BRAIN FUNCTION; COGNITION; HAPPINESS;

ADULT; AMYGDALA; BRAIN MAPPING; DISCRIMINATION (PSYCHOLOGY); EVOKED POTENTIALS; FACIAL EXPRESSION; FEAR; FEMALE; HUMANS; LINEAR MODELS; MALE; REACTION TIME; SOCIAL PERCEPTION;

EID: 79952627716     PISSN: 00283932     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2010.12.025     Document Type: Article

References (57)

1. Adolphs R. Neural systems for recognizing emotion. Current Opinion in Neurobiology 2002, 12:169-177.
2. Allison T., Puce A., Spencer D.D., McCarthy G. Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. Cerebral Cortex 1999, 9:415-430.
3. Amunts K., Kedo O., Kindler M., Pieperhoff P., Mohlberg H., Shah N.J., et al. Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: Intersubject variability and probability maps. Anatomy and Embryology 2005, 210:343-352.
4. Balconi M., Lucchiari C. Consciousness and arousal effects on emotional face processing as revealed by brain oscillations: A gamma band analysis. International Journal of Psychophysiology 2008, 67:41-46.
5. Balconi M., Pozzoli U. Arousal effect on emotional face comprehension: Frequency band changes in different time intervals. Physiology & Behavior 2009, 97:129-150.
6. Bauer E.P., Paz R., Pare D. Gamma oscillations coordinate amygdalo-rhinal interactions during learning. The Journal of Neuroscience 2007, 27:9369-9379.
7. Bayle D.J., Henaff M.A., Krolak-Salmon P. Unconsciously perceived fear in peripheral vision alerts the limbic system: A MEG study. PLoS One 2009, 4:e8207.
8. Bentin S., Allison T., Puce A., Perez E., McCarthy G. Electrophysiological studies of face perception in humans. Journal of Cognitive Neuroscience 1996, 8:551-565.
9. Bishop S.J., Jenkins R., Lawrence A.D. Neural processing of fearful faces: Effects of anxiety are gated by perceptual capacity limitations. Cerebral Cortex 2007, 17:1595-1603.
10. Breiter H.C., Etcoff N.L., Whalen P.J., Kennedy W.A., Rauch S.L., Buckner R.L., et al. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 1996, 17:875-887.
11. Critchley H., Daly E., Phillips M., Brammer M., Bullmore E., Williams S., et al. Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study. Human Brain Mapping 2000, 9:93-105.
12. Edwards E., Soltani M., Kim W., Dalal S.S., Nagarajan S.S., Berger M.S., et al. Comparison of time-frequency responses and the event-related potential to auditory speech stimuli in human cortex. Journal of Neurophysiology 2009, 102:377-386.
13. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005, 25:1325-1335.
14. Ekman P., Friesen W.V. Pictures of facial affect 1976, Consulting Psychologist, Palo Alto, CA.
15. Friston K.J., Glaser D.E., Henson R.N., Kiebel S., Phillips C., Ashburner J. Classical and Bayesian inference in neuroimaging: Applications. Neuroimage 2002, 16:484-512.
16. Friston K.J., Holmes A.P., Worsley K.J. How many subjects constitute a study?. Neuroimage 1999, 10:1-5.
17. Gorno-Tempini M.L., Pradelli S., Serafini M., Pagnoni G., Baraldi P., Porro C., et al. Explicit and incidental facial expression processing: An fMRI study. Neuroimage 2001, 14:465-473.
18. Hariri A.R., Bookheimer S.Y., Mazziotta J.C. Modulating emotional responses: Effects of a neocortical network on the limbic system. Neuroreport 2000, 11:43-48.
19. Hayasaka S., Phan K.L., Liberzon I., Worsley K.J., Nichols T.E. Nonstationary cluster-size inference with random field and permutation methods. Neuroimage 2004, 22:676-687.
20. Heath R.G., Gallant D.M. Activity of the human brain during emotional thought. The role of pleasure in behavior: A symposium by 22 authors 1964, 83-106. Harper & Row, New York. R.G. Heath (Ed.).
21. Hsu S.M., Pessoa L. Dissociable effects of bottom-up and top-down factors on the processing of unattended fearful faces. Neuropsychologia 2007, 45:3075-3086.
22. Hung Y., Smith M.L., Bayle D.J., Mills T., Cheyne D., Taylor M.J. Unattended emotional faces elicit early lateralized amygdala-frontal and fusiform activations. Neuroimage 2010, 50:727-733.
23. Johnsen B.H., Thayer J.F., Hugdahl K. Affective judgment of the Ekman faces: A dimensional approach. Journal of Psychophysiology 1995, 9:193-202.
24. Jones E.G., Burton H. A projection from the medial pulvinar to the amygdala in primates. Brain Research 1976, 104:142-147.
25. Karaka S., Baar-Eroglu C., Ozesmi C., Kafadar H., Erzengin O.U. Gamma response of the brain: A multifunctional oscillation that represents bottom-up with top-down processing. International Journal of Psychophysiology 2001, 39:137-150.
26. Keil A., Muller M.M., Gruber T., Wienbruch C., Stolarova M., Elbert T. Effects of emotional arousal in the cerebral hemispheres: A study of oscillatory brain activity and event-related potentials. Clinical Neurophysiology 2001, 112:2057-2068.
27. Kilner J.M., Kiebel S.J., Friston K.J. Applications of random field theory to electrophysiology. Neuroscience Letters 2005, 374:174-178.
28. Klopp J., Marinkovic K., Chauvel P., Nenov V., Halgren E. Early widespread cortical distribution of coherent fusiform face selective activity. Human Brain Mapping 2000, 11:286-293.
29. Krolak-Salmon P., Henaff M.A., Vighetto A., Bertrand O., Mauguiere F. Early amygdala reaction to fear spreading in occipital, temporal, and frontal cortex: A depth electrode ERP study in human. Neuron 2004, 42:665-676.
30. Lachaux J.P., Rudrauf D., Kahane P. Intracranial EEG and human brain mapping. Journal of Physiology, Paris 2003, 97:613-628.
31. Lange K., Williams L.M., Young A.W., Bullmore E.T., Brammer M.J., Williams S.C., et al. Task instructions modulate neural responses to fearful facial expressions. Biological Psychiatry 2003, 53:226-232.
32. LeDoux J.E. The emotional brain: The mysterious underpinnings of emotional life 1996, Simon & Schuster, New York.
33. Luo Q., Holroyd T., Jones M., Hendler T., Blair J. Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG. Neuroimage 2007, 34:839-847.
34. Luo Q., Mitchell D., Cheng X., Mondillo K., Mccaffrey D., Holroyd T., et al. Visual awareness, emotion, and gamma band synchronization. Cerebral Cortex 2009, 19:1896-1904.
35. Makeig S., Debener S., Onton J., Delorme A. Mining event-related brain dynamics. Trends in Cognitive Sciences 2004, 8:204-210.
36. Maratos F.A., Mogg K., Bradley B.P., Rippon G., Senior C. Coarse threat images reveal theta oscillations in the amygdala: A magnetoencephalography study. Cognitive, Affective, and Behavioral Neuroscience 2009, 9:133-143.
37. Mihara T., Baba K. Combined use of subdural and depth electrodes. Epilepsy surgery 2001, 613-621. Lippincott Williams & Wilkins, Philadelphia. 2nd ed. H.O. Luders, Y.G. Comair (Eds.).
38. Mikuni N., Nagamine T., Ikeda A., Terada K., Taki W., Kimura J., et al. Simultaneous recording of epileptiform discharges by MEG and subdural electrodes in temporal lobe epilepsy. Neuroimage 1997, 5:298-306.
39. Morris J.S., de Bonis M., Dolan R.J. Human amygdala responses to fearful eyes. Neuroimage 2002, 17:214-222.
40. Morris J.S., Frith C.D., Perrett D.I., Rowland D. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 1996, 383:812-815.
41. Morris J.S., Ohman A., Dolan R.J. A subcortical pathway to the right amygdala mediating " unseen" fear. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:1680-1685.
42. Muller M.M., Keil A., Gruber T., Elbert T. Processing of affective pictures modulates right-hemispheric gamma band EEG activity. Clinical Neurophysiology 1999, 110:1913-1920.
43. Murphy S.T., Zajonc R.B. Affect, cognition, and awareness: Affective priming with optimal and suboptimal stimulus exposures. Journal of Personality and Social Psychology 1993, 64:723-739.
44. Nomura M., Ohira H., Haneda K., Iidaka T., Sadato N., Okada T., et al. Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: An event-related fMRI study. Neuroimage 2004, 21:352-363.
45. Oldfield R.C. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
46. Oya H., Kawasaki H., Howard M.A., Adolphs R. Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. Journal of Neuroscience 2002, 22:9502-9512.
47. Papadelis C., Poghosyan V., Fenwick P.B., Ioannides A.A. MEG's ability to localise accurately weak transient neural sources. Clinical Neurophysiology 2009, 120:1958-1970.
48. Pegna A.J., Khateb A., Lazeyras F., Seghier M.L. Discriminating emotional faces without primary visual cortices involves the right amygdala. Nature Neuroscience 2005, 8:24-25.
49. Pessoa L., McKenna M., Gutierrez E., Ungerleider L.G. Neural processing of emotional faces requires attention. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:11458-11463.
50. Pessoa L., Padmala S., Morland T. Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation. Neuroimage 2005, 28:249-255.
51. Phillips M.L., Medford N., Young A.W., Williams L., Williams S.C., Bullmore E.T., et al. Time courses of left and right amygdalar responses to fearful facial expressions. Human Brain Mapping 2001, 12:193-202.
52. Popescu A.T., Popa D., Pare D. Coherent gamma oscillations couple the amygdala and striatum during learning. Nature Neuroscience 2009, 12:801-807.
53. Rossion B., Jacques C. Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170. Neuroimage 2008, 39:1959-1979.
54. Sato W., Yoshikawa S., Kochiyama T., Matsumura M. The amygdala processes the emotional significance of facial expressions: An fMRI investigation using the interaction between expression and face direction. Neuroimage 2004, 22:1006-1013.
55. Whalen P.J., Rauch S.L., Etcoff N.L., McInerney S.C., Lee M.B., Jenike M.A. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience 1998, 18:411-418.
56. Williams L.M., Phillips M.L., Brammer M.J., Skerrett D., Lagopoulos J., Rennie C., et al. Arousal dissociates amygdala and hippocampal fear responses: Evidence from simultaneous fMRI and skin conductance recording. Neuroimage 2001, 14:1070-1079.
57. Wright C.I., Fischer H., Whalen P.J., McInerney S.C., Shin L.M., Rauch S.L. Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli. Neuroreport 2001, 12:379-383.