Subcortical face processing

Nature Reviews Neuroscience

Volumn 6, Issue 10, 2005, Pages 766-774

  Johnson, Mark H ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALOID NUCLEUS; AUTISM; BRAIN CORTEX; BRAIN FUNCTION; DEVELOPMENTAL DISORDER; ELECTROPHYSIOLOGY; EVENT RELATED POTENTIAL; FACE; FACIAL EXPRESSION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMISPHERE; HUMAN; MAGNETOENCEPHALOGRAPHY; NEGLECT; NEUROIMAGING; NEUROPSYCHOLOGY; NONHUMAN; ORBITAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROSOPAGNOSIA; REVIEW; SOCIAL INTERACTION; STIMULUS RESPONSE; VISUAL CORTEX; VISUAL FIELD; VISUAL INFORMATION; VISUAL STIMULATION;

EID: 27944433009     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn1766     Document Type: Review

References (116)

1. Desmond, J. E. & Fiez, J. A. Neuroimaging studies of the cerebellum: language, learning and memory. Trends Cogn. Sci. 2, 355-362 (1998).
2. Marien, P., Engelborghs, S., Fabbro, F. & De Deyn, P. The lateralized linguistic cerebellum: a review and new hypothesis. Brain Lang. 79, 580-600 (2001).
3. Vuilleumier, P. Faces call for attention: evidence from patients with visual extinction. Neuropsychologia 38, 693-700 (2000).
4. Vuilleumier, P. & Sagiv, N. Two eyes make a pair: facial organization and perceptual learning reduce visual extinction. Neuropsychologia 39, 1144-1149 (2001).
5. Morris, J. S., de Gelder, B., Weiskrantz, L. & Dolan, R. J. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 124, 1241-1252 (2001).
6. de Gelder, B., Frissen, I., Barton, J. & Hadjikhani, N. A modulatory role for facial expressions in prosopagnosia. Proc. Natl Acad. Sci. USA 100, 13105-13110 (2003).
7. Eimer, M. & Holmes, A. An ERP study on the time course of emotional face processing. Neuroreport 13, 427-431 (2002).
8. Streit, M. et al. Time course of regional brain activations during facial emotion recognition in humans. Neurosci. Lett. 342, 101-104 (2003).
9. Braeutigam, S., Bailey, A. J. & Swithenby, S. J. Task-dependent early latency (30-60 ms) visual processing of human faces and other objects. Neuroreport 12, 1531-1536 (2001). One of several studies showing clear evidence for an early fast-track for face processing.
10. Pourtois, G., Thut, G., dePeralta, R. G., Michel, C. & Vuilleumier, P. Two electrophysiological stages of spatial orienting towards fearful faces: early temporal-parietal activation preceding gain control in the extrastriate visual cortex. Neuroimage 26, 149-163 (2005).
11. Bar, M. A cortical mechanism for triggering top-down facilitation in visual object recognition. J. Cogn. Neurosci. 15, 600-609 (2003).
12. Bailey, A. J., Braeutigam, S., Jousmaki, V. & Swithenby, S. S. Abnormal activation of face processing systems at early and intermediate latency in individuals with autism spectrum disorder: a magnetoencephalographic study. Eur. J. Neurosci. 21, 2575-2585 (2005).
13. 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 42, 665-676 (2004).
14. Livingstone, M. & Hubel, D. Segregation of form, color, movement and depth: anatomy, physiology and perception. Science 240, 740-749 (1988).
15. Merigan, W. & Maunsell, J. How parallel are the primate visual pathways? Annu. Rev. Neurosci. 16, 369-402 (1993).
16. Schiller, P. H., Malpeli, J. G. & Schein, S. J. Composition of geniculo-striate input to superior colliculus of the rhesus monkey. J. Neurophysiol. 42, 1124-1133 (1979).
17. Vuilleumier, P., Armony, J. L., Driver, J. & Dolan, R. J. Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nature Neurosci. 6, 624-631 (2003). Establishes that HSF and LSF visual information about faces is processed by distinct neural pathways - the cortical and subcortical routes, respectively.
18. Winston, J. S., Vuilleumier, P. & Dolan, R. J. Effects of low spatial frequency components of fearful faces on fusiform cortex activity. Curr. Biol. 13, 1824-1829 (2003).
19. Zald, D. H. The human amygdala and the emotional evaluation of sensory stimuli. Brain Res. Brain Res. Rev. 41, 88-123 (2003).
20. Morris, J. S. et al. A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121, 47-57 (1998).
21. Keightley, M. L. et al. An fMRI study investigating cognitive modulation of brain regions associated with emotional processing of visual stimuli. Neuropsychologia 41, 585-596 (2003).
22. Iidaka, T. et al. Neural interaction of the amygdala with the prefrontal and temporal cortices in the processing of facial expressions as revealed by fMRI. J. Cogn. Neurosci. 13, 1035-1047 (2001).
23. George, N., Driver, J. & Dolan, R. J. Seen gaze-direction modulates fusiform activity and its coupling with other brain areas during face processing. Neuroimage 13, 1102-1112 (2001).
24. Kim, H. et al. Contextual modulation of amygdala responsivity to surprised faces. J. Cogn. Neurosci. 16, 1730-1745 (2004).
25. LeDoux, J. E. The Emotional Brain (Simon & Schuster, New York, 1996).
26. Adolphs, R. & Tranel, D. Amygdala damage impairs emotion recognition from scenes only when they contain facial expressions. Neuropsychologia 41, 1281-1289 (2003).
27. Hariri, A. R., Tessitore, A., Mattay, V. S., Fera, F. & Weinberger, D. R. The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage 17, 317-323 (2002).
28. Hadjikhani, N. & de Gelder, B. Seeing fearful body expressions activates the fusiform cortex and amygdala. Curr. Biol. 13, 1-20 (2003).
29. Kesler-West, M. L. et al. Neural substrates of facial emotion processing using fMRI. Brain Res. Cogn. Brain Res. 11, 213-226 (2001).
30. Adolphs, R. et al. A mechanism for impaired fear recognition after amygdala damage. Nature 433, 22-23 (2005). Establishes that a patient with amygdala damage can successfully recognize fearful expressions if their attention is directed towards the eyes. Results suggest that amygdala damage in humans does not result in a selective fear perception deficit, but in a problem with directing attention towards the eyes of others.
31. Adams, R. B. J. et al. Effects of gaze on amygdala sensitivity to anger and fear faces. Science 300, 1536 (2003).
32. Kawashima, R. et al. The human amygdala plays an important role in gaze monitoring. Brain 122, 779-783 (1999).
33. Morris, J. S., deBonis, M. & Dolan, R. J. Human amygdala responses to fearful eyes. Neuroimage 17, 214-222 (2002).
34. Whalen, P. J. et al. Human amygdala responsivity to masked fearful eye whites. Science 306, 2061 (2004). Establishes that, at least with faces close to the viewer, the amygdala responds to the proportion of white around the pupil.
35. Johnson, M. H. & Morton, J. Biology and Cognitive Development: The Case of Face Recognition (Blackwell, Oxford, 1991).
36. Grieve, K. L., Acuna, C. & Cudeiro, J. The primate pulvinar nuclei: vision and action. Trends Neurosci. 23, 35-39 (2000).
37. Benevento, L. A. & Standage, G. P. The organization of projections of the retino-recipient and non-retino-recipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. J. Comp. Neurol. 218, 307-336 (1983).
38. Robinson, D. L. & Petersen, S. E. The pulvinar and visual salience. Trends Neurosci. 15, 127-132 (1992).
39. O'Brien, B. J., Abel, P. L. & Olavarria, J. F. The retinal input to calbindin-D28k-defined subdivisions in macaque inferior pulvinar. Neurosci. Lett. 312, 145-148 (2001).
40. Jones, E. G. & Burton, H. A projection from the medial pulvinar to the amygdala in primates. Brain Res. 104, 142-147 (1976).
41. Johnson, M. H., Dziurawiec, S., Ellis, H. D. & Morton, J. Newborns' preferential tracking of face-like stimuli and its subsequent decline. Cognition 40, 1-19 (1991).
42. Morton, J. & Johnson, M. H. CONSPEC and CONLERN: a two-process theory of infant face recognition. Psychol. Rev. 98, 164-181 (1991).
43. de Schonen, S. & Mathivet, E. First come, first served: a scenario about the development of hemispheric specialisation in face recognition during infancy. Curr. Psychol. Cogn. 9, 3-44 (1989).
44. Nelson, C. A. The development and neural bases of face recognition. Inf. Child Dev. 10, 3-18 (2001).
45. Gauthier, I. & Nelson, C. The development of face expertise. Curr. Opin. Neurobiol. 11, 219-224 (2001).
46. Macchi Cassia, V., Simion, F. & Umiltà, C. Face preference at birth: the role of an orienting mechanism. Dev. Sci. 4, 101-108 (2001).
47. Simion, F., Macchi Cassia, V., Turati, C. & Valenza, E. in The Development of Face Processing in Infancy and Early Childhood: Current Perspectives (eds Pascalis, O. & Slater, A.) 13-26 (Nova Science, New York, 2003).
48. Turati, C., Simion, F., Milani, I. & Umiltà, C. Newborns' preference for faces: what is crucial? Dev. Psychol. 38, 875-888 (2002).
49. Farroni, T., Johnson, M. H., Zulian, L. & Csibra, G. unpublished observations.
50. de Haan, M., Humphrey, K. & Johnson, M. H. Developing a brain specialized for face perception: a converging methods approach. Dev. Psychobiol. 40, 200-212 (2002).
51. Atkinson, J. The Developing Visual Brain (Oxford Univ. Press, Oxford, 2000).
52. Born, A. P., Rostrup, E., Miranda, M. J., Larsson, H. B. W. & Lou, H. C. Visual cortex reactivity in sedated children examined with perfusion MRI (FAIR). Magn. Reson. Imaging 20, 199-205 (2002).
53. Johnson, M. H. Cortical maturation and the development of visual attention in early infancy. J. Cogn. Neurosci. 2, 81-95 (1990).
54. Csibra, G., Tucker, L. A., Volein, A. & Johnson, M. H. Cortical development and saccade planning: the ontogeny of the spike potential. Neuroreport 11, 1069-1073 (2000).
55. Sewards, T. V. & Sewards, M. A. Innate visual object recognition in vertebrates: some proposed pathways and mechanisms. Comp. Biochem. Physiol. A 132, 861-891 (2002). A useful review of evidence for subcortical conspecific detection in the young of several vertebrate species.
56. Horn, G. Pathways of the past; the imprint of memory. Nature Rev. Neurosci. 5, 108-120 (2004).
57. Rafal, R., Henik, A. & Smith, J. Extrageniculate contributions to reflex visual orienting in normal humans - a temporal hemifield advantage. J. Cogn. Neurosci. 3, 323-329 (1992).
58. de Gelder, B. & Stekelenburg, J. J. Nasal-temporal asymmetry of the N170 for processing faces in normal viewers but not in developmental prosopagnosia. Neurosci. Lett. 376, 40-45 (2005).
59. Simion, F., Valenza, E., Umiltà, C. & Dalla Barba, B. Inhibition of return in newborns is temporo-nasal asymmetrical. Inf. Behav. Dev. 18, 189-194 (1995).
60. Simion, F., Valenza, E., Umiltà, C. & Dalla Barba, B. Preferential orienting to faces in newborns: a temporal-nasal asymmetry. J. Exp. Psychol. Hum. Percept. Perform. 24, 1399-1405 (1998). An important demonstration that the newborn preference for face-related patterns is due to temporal visual field input. As the temporal field feeds preferentially into the subcortical visual pathway, this supports the view that these preferences are mediated by structures in this circuit.
61. Farroni, T., Simion, F., Umiltà, C. & Dalla Barba, B. The gap effect in newborns. Dev. Sci. 2, 174-186 (1999).
62. Adolphs, R. Cognitive neuroscience of human social behaviour. Nature Rev. Neurosci. 4, 165-178 (2003).
63. Johnson, M. H. Developmental Cognitive Neuroscience: An Introduction 2nd edn (Blackwell, Oxford, 2005).
64. Bentley, P., Vuilleumier, P., Thiel, C. M., Driver, J. & Dolan, R. J. Cholinergic enhancement modulates neural correlates of selective attention and emotional processing. Neuroimage 20, 58-70 (2003).
65. Dorner, G., Bluth, R. & Tonjes, R. Acetylcholine concentrations in the developing bran appear to affect emotionality and mental capacity in later life. Acta Biol. Med. Ger. 41, 721-723 (1982).
66. Thomas, K. M. et al. Amygdala response to facial expressions in children and adults. Biol. Psychiatry 49, 309-316 (2001).
67. Cunningham, M. G., Bhattacharyya, S. & Benes, F. M. Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J. Comp. Neurol. 453, 116-130 (2002).
68. Skuse, D., Morris, J. & Lawrence, K. The amygdala and development of the social brain. Ann. NY Acad. Sci. 1008, 91-101 (2003).
69. Lawrence, K., Kuntsi, J., Coleman, M., Campbell, R. & Skuse, D. Face and emotion recognition deficits in Turner syndrome: a possible role for X-linked genes in amygdala development. Neuropsychology 17, 39-49 (2003).
70. Meyer-Lindenberg, A. et al. Neural correlates of genetically abnormal social cognition in Williams syndrome. Nature Neurosci. 8, 991-993 (2005).
71. Bauman, M. & Kemper, T. Limbic and cerebellar abnormalities: consistent findings in infantile autism. J. Neuropathol. Exp. Neurol. 47, 369 (1988).
72. Brothers, L., Ring, B. & Kling, A. Responses of neurons in the macaque amygdala to complex social stimuli. Behav. Brain Res. 41, 199-213 (1990).
73. Baron-Cohen, S. et al. The amygdala theory of autism. Neurosci. Biobehav. Rev. 24, 355-364 (2000). This important review presents evidence in support of a disturbance of the amygdala in ASD.
74. Abell, F. et al. The neuroanatomy of autism: a voxel based whole brain analysis of structural MRI scans in high functioning individuals. Neuroreport 10, 1647-1651 (1999).
75. Bachevalier, J. in Advances in Neuropsychiatry and Psychopharmacology: Volume 1. Schizophrenia Research (eds Tamminga, C. & Schulz, S.) 129-140 (Raven, New York, 1991).
76. Stone, V. E., Baron-Cohen, S., Calder, A., Keane, J. & Young, A. Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia 41, 209-220 (2003).
77. Ogai, M. et al. fMRI study of recognition of facial expressions in high-functioning autistic patients. Neuroreport 14, 559-563 (2003).
78. Hall, G. B., Szechtman, H. & Nahmias, C. Enhanced salience and emotion recognition in autism: a PET study. Am. J. Psychiatry 160, 1439-1441 (2003).
79. Schultz, R. T. et al. The role of the fusiform face area in social cognition: implications for the pathobiology of autism. Phil. Trans. R. Soc. Lond. B 358, 415-427 (2003).
80. Baron-Cohen, S. et al. Social intelligence in the normal and autistic brain: an fMRI study. Eur. J. Neurosci. 11, 1891-1898 (1999).
81. Bauman, M. L. & Kemper, T. L. The Neurobiology of Autism 2nd edn (John Hopkins Univ. Press, Baltimore, 2005).
82. Grice, S. J. et al. Neural correlates of eye-gaze detection in young children with autism. Cortex 41, 342-353 (2005).
83. Happe, F. Autism: cognitive deficit or cognitive style? Trends Cogn. Sci. 3, 216-222 (1999).
84. Deruelle, C., Rondan, C., Gepner, B. & Tardif, C. Spatial frequency and face processing in children with autism and Asperger syndrome. J. Autism Dev. Disord. 34, 199-210 (2004).
85. Dawson, G., Webb, S. J. & McPartland, J. Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev. Neuropsychol. 27, 403-424 (2005).
86. Bentin, S., Deouell, L. & Soroker, N. Selective streaming of visual information in face recognition: evidence from congenital prosopagnosia. Neuroreport 10, 823-827 (1999).
87. Farah, M. J., Rabinowitz, C., Quinn, G. E. & Liu, G. T. Early commitment of neural substrates for race recognition. Cogn. Neuropsychol. 17, 117-123 (2000).
88. Jones, R. D. & Tranel, D. Severe developmental prosopagnosia in a child with superior intellect. J. Clin. Exp. Neuropsychol. 23, 265-273 (2001).
89. Nunn, J. A., Postma, P. & Pearson, R. Developmental prosopagnosia: should it be taken at face value? Neurocase 7, 15-27 (2001).
90. Behrmann, M. & Avidan, G. Congenital prosopagnosia: face-blind from birth. Trends Cogn. Sci. 9, 180-187 (2005).
91. Barton, J. J. S., Cherkasova, M. V. & O'Connor, M. Covert recognition in acquired and developmental prosopagnosia. Neurology 57, 1161-1168 (2001).
92. Simion, F., Macchi-Cassia, V., Turati, C. & Valenza, E. The origins of face perception: specific versus non-specific mechanisms. Inf. Child Dev. 10, 59 (2001).
93. Simion, F. et al. Newborns' local processing in schematic facelike configurations. Br. J. Dev. Psychol. 14, 257-273 (2002).
94. Slater, A. et al. Newborn infants' preference for attractive faces: the role of internal and external facial features. Infancy 1, 265-274 (2000).
95. Slater, A., Von der Schulenburg, C., Brown, E. & Badenoch, M. Newborn infants prefer attractive faces. Inf. Behav. Dev. 21, 345-354 (1998).
96. Tzourio-Mazoyer, N. et al. Neural correlates of woman face processing by 2-month-old infants. Neuroimage 15, 454-461 (2002).
97. Halit, H., Csibra, G., Volein, Á. & Johnson, M. H. Face-sensitive cortical processing in early infancy. J. Chid Psychol. Psychiatry 45, 1228-1234 (2004).
98. Ghashghaei, H. & Barbas, H. Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115, 1261-1279 (2002).
99. Batki, A., Baron-Cohen, S., Wheelwright, S., Connellan, J. & Ahluwalia, J. Is there an innate gaze module? Evidence from human neonates. Inf. Behav. Dev. 23, 223-229 (2000).
100. Bushnell, I. W. R., Sai, F. & Mullin, J. T. Neonatal recognition of the mother's face. Brit. J. Dev. Psychol. 7, 3-15 (1989).
101. Easterbrook, M., Hains, S., Muir, D. & Kisilevsky, B. Faceness or complexity: evidence from newborn visual tracking of facelike stimuli. Inf. Behav. Dev. 22, 17-35 (1999).
102. Farroni, T., Csibra, G., Simion, F. & Johnson, M. H. Eye contact detection in humans from birth. Proc. Natl Acad. Sci. USA 99, 9602-9605 (2002).
103. Farroni, T., Pividori, D., Simion, F., Massaccesi, S. & Johnson, M. H. Eye gaze cueing of attention in newborns. Infancy 5, 39-60 (2004).
104. Macchi-Cassia, V., Turati, C. & Simion, F. Can a non-specific bias toward top-heavy patterns explain newborn preference? Psychol. Sci. 15, 379-383 (2004).
105. Pascalis, O. & de Schonen, S. Recognition memory in 3- to 4-day-old human neonates. Neuroreport 5, 1721-1724 (1994).
106. Umiltà, C., Simion, F. & Valenza, E. Newborn's preference for faces. Eur. Psychol. 1, 200-205 (1996).
107. Walton, G., Bower, N. & Bower, T. Recognition of familiar faces by newborns, Inf. Behav. Dev. 15, 265-269 (1992).
108. Kleiner, K. A. & Banks, M. S. Stimulus energy does not account for 2-month-old's preferences. J. Exp. Psychol. Hum. Percept. Perform. 13, 594-600 (1987).
109. Morton, J., Johnson, M. H. & Maurer, D. On the reasons for newborns' responses to faces. Inf. Behav. Dev. 13, 99-103 (1990).
110. Acerra, F., Burnod, Y. & de Schonen, S. Modelling aspects of face processing in early infancy. Dev. Sci. 5, 98-117 (2002).
111. Bednar, J. A. & Miikkulainen, R. Learning innate face preferences. Neural Comput. 15, 1525-1557 (2003).
112. Quinn, P. C. & Slater, A. in Face Perception in infancy and Early Childhood: Current Perspectives (eds Pascalis, O. & Slater, A.) 3-11 (NOVA Science, New York, 2003).
113. Langlois, J. H. & Roggman, L. A. Attractive faces are only average. Psychol. Sci. 1, 115-121 (1990).
114. Gauthier, I., Tarr, M. J., Anderson, A. W., Skudlarski, P. & Gore, J. C. Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects. Nature Neurosci. 2, 574-580 (1999).
115. Malach, R., Avidan, G., Lerner, Y., Hasson, U. & Levy, I. in Attention and Performance XX (eds Kanishwer, N. & Duncan, J.) 195-204 (Oxford Univ. Press, Oxford, 2004).
116. Sun, T. et al. Early asymmetry of gene transcription in embryonic human left and right cerebral cortex. Science 308, 1794-1798 (2005).