Dissociable neural pathways are involved in the recognition of emotion in static and dynamic facial expressions

NeuroImage

Volumn 18, Issue 1, 2003, Pages 156-168

  Kilts, Clinton D ^a   Egan, Glenn ^a   Gideon, Deborah A ^a   Ely, Timothy D ^a   Hoffman, John M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biological motion; Dynamic and static stimuli; Facial expressions of emotion; Positron emission tomography (PET); Social perception

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ANGER; ARTICLE; BRAIN FUNCTION; BRAIN REGION; BRAIN STEM; CEREBELLUM; CONTROLLED STUDY; CORRELATION ANALYSIS; CUNEATE NUCLEUS; EMOTION; FACIAL EXPRESSION; FEMALE; FRONTAL CORTEX; HAPPINESS; HEMISPHERIC DOMINANCE; HUMAN; HUMAN EXPERIMENT; IMAGERY; MALE; MOTOR CORTEX; NERVE CELL; NERVE CELL NETWORK; NORMAL HUMAN; PARIETAL LOBE; PERCEPTION; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIORITY JOURNAL; SPATIAL ORIENTATION; STIMULATION; STRIATE CORTEX; TEMPORAL CORTEX; VISUAL CORTEX;

EID: 0037226907     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1006/nimg.2002.1323     Document Type: Article

References (79)

1. Adolphs, R., Tranel, D., Damasio, H., and Damasio. A. R. 1994. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372: 669-672.
2. Adolphs, R., Tranel, D., Hamann, S., Young, A. W., Calder, A. J., Phelps, E. A., Anderson, A., Lee, G. P., and Damasio, A. R. 1999. Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia 37: 1111-1117.
3. Adolphs, R., Damasio, H., Tranel, D., Cooper, G., and Damasio, A. R. 2000. A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. J. Neurosci. 20: 2683-2690.
4. Adolphs, R. 2002. Neural systems for recognizing emotion. Curr. Opin. Neurobiol. 12: 169-177.
5. Allison, T., Puce, A., and McCarthy, G. 2000. Social perception from visual cues: Role of the STS region. Trends Cogn. Sci. 4: 267-278.
6. Archer, J., Hay, D. C., and Young, A. W. 1992. Face processing in psychiatric conditions. Br. J. Clin. Psychol. 31: 45-61.
7. Archer, J., and Hay, D. C. 1994. Movement, face processing and schizophrenia: Evidence of a differential deficit in expression analysis. Br. J. Clin. Psychol. 33: 517-528.
8. Aronoff, J., Woike, B. A., and Hyman, L. M. 1992. Which are the stimuli in facial displays of anger and happiness? Configurational bases of emotion recognition. J. Pers. Soc. Psychol. 62: 1050-1066.
9. Barceló, F., Suwazono, S., and Knight, R. T. 2000. Prefrontal modulation of visual processing in humans. Nat. Neurosci. 3: 399-403.
10. Berns, G. S., McClure, S. M., Pagnoni, G., and Montague, P. R. 2001. Predictability modulates human brain response to reward. J. Neurosci. 21: 2793-2798.
11. Binkofski, F., Amunts, K., Stephan, K. M., Posse, S., Schormann, T., Freund, H. J., Lilles, K., and Seitz. R. J. 2000. Broca's region subserves imagery of motion: A combined cytoarchitectonic and fMRI study. Hum. Brain Mapp. 11: 273-285.
12. Blair, R. J. R., Morris, J. S., Frith, C. D., Perrett, D. I., and Dolan, R. J. 1999. Dissociable neural responses to facial expressions of sadness and anger. Brain 122: 883-893.
13. Bonda, E., Petrides, M., Frey, S., and Evans, A. 1995. Neural correlates of mental transformations of the body-in-space. Proc. Natl. Acad. Sci. USA 92: 11180-11184.
14. Bonda, E., Petrides, M., Ostry, D., and Evans, A. 1996. Specific involvement of human parietal systems and the amygdala in the perception of biological motion. J. Neurosci. 16: 3737-3744.
15. Borod, J. C., Martin, C. C., Alpert, M., Brozgold, A., and Welkowitz, J. 1993. Perception of facial emotion in schizophrenia and right brain-damaged patients. J. Nerv. Ment. Dis. 181: 494-502.
16. Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., Strauss, M. M., Hyman, S. E., and Rosen, B. R. 1996. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17: 875-887.
17. Calder, A. J., Lawrence, A. D., and Young, A. W. 2001. Neuropsychology of fear and loathing. Nature Rev. 2: 352-363.
18. Chawla, D., Rees, G., and Friston, K. J. 1999. The physiological basis of attentional modulation in extrastriate visual areas. Nature Neurosci. 2: 671-676.
19. Cherry, S. R., Woods, R. P., Hoffman, E. J., and Mazziotta, J. C. 1993. Improved detection of focal cerebral blood-flow changes using 3-dimensional positron emission tomography. J. Cereb. Blood Flow Metab. 13: 630-638.
20. Cohen, M. S., Kosslyn, S. M., Breiter, H. C., DiGirolamo, G. J., Thompson, W. L., Anderson, A. K., Bookheimer, S. Y., Rosen, B. R., and Belliveau, J. W. 1996. Changes in cortical activity during mental rotation: A mapping study using functional MRI. Brain 119: 89-100.
21. Critchley, H. D., Daly, E. M., Bullmore, E. T., Williams, S. C. R., Van Amelsvoort, T., Robertson, D. M., Rowe, A., Phillips, M., McAlonan, G., Howlin, P., and Murphy, D. G. M. 2000a. The functional neuroanatomy of social behaviour: Changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 123: 2203-2212.
22. Critchley, H., Daly, E., Phillips, M., Brammer, M., Bullmore, E., Williams, S., Van Amelsvoort, T., Robertson, D., David, A., and Murphy, D. 2000b. Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study. Hum. Brain. Mapp. 9: 93-105.
23. Decety, J., and Grèzes, J. 1999. Neural mechanisms subserving the perception of human actions. Trends Cogn. Sci. 3: 172-178.
24. Desimone, R. 1991. Face-selective cells in the temporal cortex of monkeys. J. Cogn. Neurosci. 3: 1-8.
25. Desimone, R., and Duncan, J. 1995. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18: 193-222.
26. Dimberg, U., Thunberg, M., and Elmehed, K. 2000. Unconscious facial reactions to emotional facial expressions. Psychol. Sci. 11: 86-89.
27. Ekman, P. 1982. Emotion in the Human Face, 2nd Ed. Cambridge Univ. Press, Cambridge, England.
28. Farah, M. J., Levison, K. L., and Klein, K. L. 1995. Face perception and within-category discrimination in prosopagnosia. Neuropsychologia 33: 661-674.
29. Gallagher, H. L., Happè, F., Brunswick, N., Fletcher, P. C., Frith, U., and Frith, C. D. 2000. Reading the mind in cartoons and stories: An fMRI study of the 'theory of mind' in verbal and nonverbal tasks. Neuropsychologia 38: 11-21.
30. Gauthier, I., Tarr, M. J., Anderson, A. W., Skudlarski, P., and Gore, J. C. 1999. Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects. Nature Neurosci. 2: 568-573.
31. Gerardin, E., Sirigu, A., Lehéricy, S., Poline, J. B., Gaymard, B., Marsault, C., Agid, Y., and Le Bihan, D. 2000. Partially overlapping neural networks for real and imagined hand movements. Cereb. Cortex 10: 1093-1104.
32. Gorno-Tempini, M., Pradelli, S., Serafini, M., Pagnoni, G., Baraldi, P., Porro, C., Nicoletti, R., Umita, C., and Nichelli, P. 2001. Explicit and incidental facial expression processing: An fMRI study. NeuroImage 14: 465-473.
33. Grèzes, J., Fonlupt, P., Bertenthal, B., Delon-Martin, C., Segebarth, C., and Decety, J. 2001. Does perception of biological motion rely on specific brain regions? NeuroImage 13: 775-785.
34. Grossman, E., Donnelly, M., Price, R., Pickens, D., Morgan, V., Neighbor, G., and Blake, R. 2000. Brain areas involved in perception of biological motion. J. Cogn. Neurosci. 12: 711-720.
35. Hargrave, R., Maddock, R. J., and Stone, V. 2002. Impaired recognition of facial expressions of emotions in Alzheimer's disease. J. Neuropsych. Clin. Neurosci. 14: 64-71.
36. Harries, M. H., and Perrett, D. I. 1991. Visual processing of faces in temporal cortex: Physiological evidence for a modular organization and possible anatomical correlates. J. Cogn. Neurosci. 3: 9-24.
37. Haxby, J. V., Horwitz, B., Ungerleider, L. G., Maisog, J. M., Pietrini, P., and Grady, C. L. 1994. The functional organization of human extrastriate cortex: A PET-rCBF study of selective attention to faces and locations. J. Neurosci. 14: 6336-6353.
38. Haxby, J. V., Hoffman, E. A., and Gobbini, M. I. 2000. The distributed human neural system for face perception. Trends Cogn. Sci. 4: 223-233.
39. Hill, H., and Johnston, A. 2001. Categorizing sex and identity from the biological motion of faces. Curr. Biol. 11: 880-885.
40. Humphreys, G. W., Donnelly, N., and Riddoch, M. J. 1993. Expression is computed separately from facial identity, and it is computed separately for moving and static faces: Neuropsychological evidence. Neuropsychologia 31: 173-181.
41. Jeannerod, M., and Decety, J. 1995. Mental motor imagery: A window into the representational stages of action. Curr. Opin. Neurobiol. 5: 727-732.
42. Jeannerod, M., and Frak, V. 1999. Mental imaging of motor activity in humans. Curr. Opin. Neurobiol. 9: 735-739.
43. Johansson, G. 1973. Visual perception of biological motion and a model for its analysis. Percept. Psychophys. 14: 201-211.
44. Kanwisher, N., McDermott, J., and Chun, M. M. 1997. The fusiform face area: A module in human extrastriate cortex specialized for face perception. J. Neurosci. 17: 4302-4311.
45. Kawashima, R., Sugiura, M., Kato, T., Nakamura, A., Hatano, K., Ito, K., Fukuda, H., Kojima, S., and Nakamura, K. 1999. The human amygdala plays an important role in gaze monitoring. Brain 122: 779-783.
46. Kerr, S. L., and Neale, J. M. 1993. Emotion perception in schizophrenia: Specific deficit or further evidence of generalized poor performance. J. Abn. Psychol. 102: 312-318.
47. Kohler, C. G., Bilker, W., Hagendoorn, M., Gur, R. E., and Gur, R. C. 2000. Emotion recognition deficit in schizophrenia: Association with symptompology and cognition. Biol. Psych. 48: 127-136.
48. Lemay, G., Kirouac, G., and Lacouture, Y. 1995. Expressions facials émotionelles spontanées: Dynamiques et statiques: Comparaison d'études de jegement catégoriel et dimensionel [Dynamic and static emotional facial expressions: A comparison of categorical and dimensional judgment studies]. Can. J. Behav. Sci. 27: 125-139.
49. Leonard, C. M., Voeller, K. K. S., and Kuldau, J. M. 1991. When's a smile a smile? Or how to detect a message by digitizing the signal. Psychol. Sci. 2: 166-172.
50. Lotze, M., Montoya, P., Erb, M., Hülsmann, E., Flor, H., Klose, U., Birbaumer, N., and Grodd, W. 1999. Activation of cortical and cerebellar motor areas during executed and imagined hand movements: An fMRI study. J. Cogn. Neurosci. 11: 491-501.
51. Mazziotta, J. C., Huang, S. C., and Phelphs, M. E. 1985. A noninvasive positron emission tomography technique using oxygen-15-labeled water for the evaluation of neurobehavioral task batteries. J. Cereb. Blood Flow Metab. 5: 70-78.
52. McCarthy, G. 1995. Brain activation associated with visual motion studied by functional magnetic resonance imaging in humans. Hum. Brain. Mapp. 2: 234-243.
53. Miller, E. K. 1999. The prefrontal cortex: Complex neural properties for complex behavior. Neuron 22: 15-17.
54. Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., and Dolan, R. J. 1996. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383: 812-815.
55. Neter, J., Kutner, M. H., Nachtsheim, C. J., and Wasserman, W. 1996. Applied Linear Statistical Models. Irwin, Chicago.
56. Parsons, L. M., Fox, P. T., Downs, J. H., Glass, T., Hirsch, T. B., Martin, C. C., Jerabek, P. A., and Lancaster, J. L. 1995. Use of implicit motor imagery for visual shape discrimination as revealed by PET. Nature 375: 54-58.
57. Phillips, M. L., and David, A. S. 1994. Understanding the symptoms of schizophrenia using visual scan paths. Br. J. Psychiatry 165: 673-675
58. Phillips, M. L., Young, A., Senior, C., Brammer, M., Andrew, C., Calder, A., Bullmore, E., Rowland, D., Perrett, D., Williams, S., Gray, J., and David, A. 1997. A specific neural substrate for perceiving facial expressions of disgust. Nature 389: 495-498.
59. Phillips, M. L., Bullmore, E. T., Howard, R., Woodruff, P. W. R., Wright, I. C., Williams, S. C. R., Simmons, A., Andrew, C., Brammer, M., and David, A. S. 1998. Investigation of facial recognition memory and happy and sad facial expression perception: An fMRI study. Psychiatry Res. Neuroimag. 83: 127-138.
60. Phillips, M. L., Williams, L., Senior, C., Bullmore, E. T., Brammer, M. J., Andrew, C., Williams, S. C. R., and David, A. S. 1999. A differential neural response to threatening and non-threatening negative facial expressions in paranoid and non-paranoid schizophrenics. Psychiatry Res. Neuroimag. 92: 11-31.
61. Pierce, K., Muller, R.-A., Ambrose, J., Allen, G., and Courchesne, E. 2001. Face processing occurs outside the fusiform 'face area' in autism: Evidence from functional MRI. Brain 124: 2059-2073.
62. Price, C. J., and Friston, K. J. 1997. Cognitive conjunction: A new approach to brain activation experiments. NeuroImage 5: 261-270.
63. Puce, A., Allison, T., Asgari, M., Gore, J. C., and McCarthy, G. 1996. Differential sensitivity of human visual cortex to faces, letter-strings, and textures: A functional magnetic resonance imaging study. J. Neurosci. 16: 5205-5215.
64. Puce, A., Allison, T., Bentin, S., Gore, J. C., and McCarthy, G. 1998. Temporal cortex activation in humans viewing eye and mouth movements. J. Neurosci. 18: 2188-2199.
65. Puce, A., Smith, A., and Allison, T. 2000. ERPs evoked by viewing facial movements. Cogn. Neuropsychol. 17: 221-229.
66. Rees, G., Friston, K., and Koch, C. 2000. A direct quantitative relationship between the functional properties of human and macaque V5. Nat. Neurosci. 3: 716-723.
67. Rolls, E. T. 2000. The orbitofrontal cortex and reward. Cereb. Cortex 10: 284-294.
68. Sergent, J., Ohta, S., and MacDonald, B. 1992. Functional neuroanatomy of face and object processing: A positron emission tomography study. Brain 115: 15-36.
69. Singh, S. D., Ellis, C. R., Winton, A. S. W., Singh, N. N., Leung, J. P., and Oswald, D. P. 1998. Recognition of facial expressions of emotion by children with attention deficit hyperactivity disorder. Behav. Modif. 22: 128-142.
70. Talairach, J., and Tournoux, P. 1988. Co-planar Stereotaxic Atlas of the Human Brain. Stuttgart, Thieme.
71. Tootell, R. B. H., and Taylor, J. B. 1995. Anatomical evidence for MT and additional cortical visual areas in humans. Cereb. Cortex 5: 39-55
72. Waters, K., and Terzopoulos, D. 1990. A physical model of facial tissue and muscle articulation. IEEE 77-82.
73. Watson, J. D. G., Myers, R., Frackowiak, R. S. J., Hajnal, J. V., Woods, R. P., Mazziotta, J. C., Shipp, S., and Zeki, S. 1993. Area V5 of the human brain: Evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb. Cortex 3: 79-94.
74. Werhle, T., Kaiser, S., Schmidt, S., and Scherer, K. R. 2000. Studying the dynamics of emotional expression using synthesized facial muscle movements. J. Pers. Soc. Psychol. 78: 105-119.
75. Whalen, P. J. 1998. Fear, vigilance and ambiguity: Initial neuroimaging studies of the human amygdala. Curr. Direct. Psychol. Sci. 7: 177-188.
76. Whalen, P. J., Shin, L. M., McInerney, S. C., Fischer, H., Wright, C. I., and Rauch, S. L. 2001. A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion 1: 70-83.
77. Wright, C. I., Martis, B., Shin, L. M., Fischer, H., and Rauch, S. 2002. Enhanced amygdala responsses to emotional versus neutral schematic facial expressions. Brain Imag. 13: 785-790.
78. Zacks, J., Rypma, B., Gabrieli, J. D. E., Tversky, B., and Glover, G. H. 1999. Imagined transformations of bodies: An fMRI investigation. Neuropsychologia 37: 1029-1040.
79. Zeki, S., Watson, J. D. G., Lueck, C. J., Friston, K. J., Kennard, C., and Frackowiak, R. S. J. 1991. A direct demonstration of functional specialization in human visual cortex. J. Neurosci. 11: 641-649.