The functional architecture for face-processing expertise: FMRI evidence of the developmental trajectory of the core and the extended face systems

Neuropsychologia

Volumn 51, Issue 13, 2013, Pages 2893-2908

  Haist, Frank ^a,b   Adamo, Maha ^b   Han Wazny, Jarnet ^b   Lee, Kang ^c   Stiles, Joan ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Brain development; Core and extended face networks; Functional MRI; Fusiform face area: face processing expertise

Indexed keywords

ADOLESCENT; ADULT; ADULTHOOD; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BRAIN DEVELOPMENT; BRAIN SIZE; CHILD; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; FUNCTIONAL ANATOMY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM FACE AREA; FUSIFORM GYRUS; HUMAN; INFERIOR FRONTAL GYRUS; INSULA; MALE; NEUROANATOMY; PARIETAL CORTEX; PRESCHOOL CHILD; SCHOOL CHILD; TEMPORAL LOBE; TREND STUDY;

BRAIN DEVELOPMENT; CORE AND EXTENDED FACE NETWORKS; FFA; FG; FUNCTIONAL MRI; FUSIFORM FACE AREA(S); FUSIFORM FACE AREA: FACE PROCESSING EXPERTISE; FUSIFORM GYRUS; OCCIPITAL FACE AREA; OFA; STS; SUPERIOR TEMPORAL SULCUS; VENTRAL OCCIPITOTEMPORAL CORTEX; VOT;

ADOLESCENT; ADULT; AGING; ANALYSIS OF VARIANCE; BRAIN; BRAIN MAPPING; CHILD; FACE; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; REACTION TIME; YOUNG ADULT;

EID: 84886306757     PISSN: 00283932     EISSN: 18733514     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2013.08.005     Document Type: Article

References (112)

1. Adamo M., Han J., Haist F. Denoising developmental FMRI data: Removal of structured noise from a passive-viewing task differentially impacts children and adults. Journal of Vision 2011, 11:417. (417).
2. Aristotle (350 B.C.E.). Politics. In The internet classics archive.
3. Avidan G., Behrmann M. Functional MRI reveals compromised neural integrity of the face processing network in congenital prosopagnosia. Current Biology 2009, 19:1146-1150.
4. Aylward E.H., Park J.E., Field K.M., Parsons A.C., Richards T.L., Cramer S.C., et al. Brain activation during face perception: Evidence of a developmental change. Journal of Cognitive Neuroscience 2005, 17:308-319.
5. Beauchamp M.S. Detection of eye movements from fMRI data. Magnetic Resonance in Medicine 2003, 49:376-380.
6. Beckmann C.F., Smith S.M. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Transactions on Medical Imaging 2004, 23:137-152.
7. Behrmann M., Avidan G. Congenital prosopagnosia: Face-blind from birth. Trends in Cognitive Sciences 2005, 9:180-187.
8. Berman M.G., Park J., Gonzalez R., Polk T.A., Gehrke A., Knaffla S., et al. Evaluating functional localizers: The case of the FFA. Neuroimage 2010, 50:56-71.
9. Brambati S.M., Benoit S., Monetta L., Belleville S., Joubert S. The role of the left anterior temporal lobe in the semantic processing of famous faces. Neuroimage 2010, 53:674-681.
10. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network: Anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences 2008, 1124:1-38.
11. Bushnell I.W., Sai F., Mullin J.T. Neonatal recognition of the mother's face. British Journal of Developmental Psychology 1989, 7:3-15.
12. Bzdok D., Langner R., Hoffstaedter F., Turetsky B.I., Zilles K., Eickhoff S.B. The modular neuroarchitecture of social judgments on faces. Cerebral Cortex 2012, 22:951-961.
13. Cantlon J.F., Pinel P., Dehaene S., Pelphrey K.A. Cortical representations of symbols, objects, and faces are pruned back during early childhood. Cerebral Cortex 2011, 21:191-199.
14. Cassia V.M., Turati C., Simion F. Can a nonspecific bias toward top-heavy patterns explain newborns' face preference?. Psychological Science 2004, 15:379-383.
15. Cohen L.B., Cashon C.H. Do 7-month-old infants process independent features or facial configurations?. Infant and Child Development 2001, 10:83-92.
16. Cohen M.S. Parametric analysis of fMRI data using linear systems methods. Neuroimage 1997, 6:93-103.
17. Cohen Kadosh K., Cohen Kadosh R., Dick F., Johnson M.H. Developmental changes in effective connectivity in the emerging core face network. Cerebral Cortex 2011, 21:1389-1394.
18. Cohen Kadosh K., Henson R.N., Cohen Kadosh R., Johnson M.H., Dick F. Task-dependent activation of face-sensitive cortex: An fMRI adaptation study. Journal of Cognitive Neuroscience 2010, 22:903-917.
19. Cohen Kadosh K., Johnson M.H., Dick F., Cohen Kadosh R., Blakemore S.J. Effects of age, task performance, and structural brain development on face processing. Cerebral Cortex 2013, 23:1630-1642.
20. Cox R.W., Hyde J.S. Software tools for analysis and visualization of fMRI data. NMR in Biomedicine 1997, 10:171-178.
21. de Haan M., Humphreys K., Johnson M.H. Developing a brain specialized for face perception: A converging methods approach. Developmental Psychobiology 2002, 40:200-212.
22. de Haan M., Pascalis O., Johnson M.H. Specialization of neural mechanisms underlying face recognition in human infants. Journal of Cognitive Neuroscience 2002, 14:199-209.
23. Epstein R.A., Higgins J.S., Parker W., Aguirre G.K., Cooperman S. Cortical correlates of face and scene inversion: A comparison. Neuropsychologia 2006, 44:1145-1158.
24. Fair D.A., Cohen A.L., Dosenbach N.U., Church J.A., Miezin F.M., Barch D.M., et al. The maturing architecture of the brain's default network. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:4028-4032.
25. Fairhall S.L., Ishai A. Effective connectivity within the distributed cortical network for face perception. Cerebral Cortex 2007, 17:2400-2406.
26. Forman S.D., Cohen J.D., Fitzgerald M., Eddy W.F., Mintun M.A., Noll D.C. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magnetic Resonance in Medicine 1995, 33:636-647.
27. Freire A., Lee K. Face recognition in 4- to 7-year-olds: Processing of configural, featural, and paraphernalia information. Journal of Experimental Child Psychology 2001, 80:347-371.
28. Friston K.J., Harrison L., Penny W. Dynamic causal modelling. Neuroimage 2003, 19:1273-1302.
29. Gathers A.D., Bhatt R., Corbly C.R., Farley A.B., Joseph J.E. Developmental shifts in cortical loci for face and object recognition. Neuroreport 2004, 15:1549-1553.
30. Gauthier I., Curby K.M., Skudlarski P., Epstein R.A. Individual differences in FFA activity suggest independent processing at different spatial scales. Cognitive, Affective & Behavioral Neuroscience 2005, 5:222-234.
31. Gauthier I., Tarr M.J., Moylan J., Anderson A.W., Skudlarski P., Gore J.C. Does visual subordinate-level categorisation engage the functionally defined fusiform face area?. Cognitive Neuropsychology 2000, 17:143-164.
32. Gobbini M.I., Haxby J.V. Neural systems for recognition of familiar faces. Neuropsychologia 2007, 45:32-41.
33. Golarai G., Ghahremani D.G., Whitfield-Gabrieli S., Reiss A., Eberhardt J.L., Gabrieli J.D., et al. Differential development of high-level visual cortex correlates with category-specific recognition memory. Nature Neuroscience 2007, 10:512-522.
34. Golarai G., Liberman A., Yoon J.M., Grill-Spector K. Differential development of the ventral visual cortex extends through adolescence. Frontiers in Human Neuroscience 2010, 3:80.
35. Grill-Spector K., Knouf N., Kanwisher N. The fusiform face area subserves face perception, not generic within-category identification. Nature Neuroscience 2004, 7:555-562.
36. Haist F., Adamo M., Westerfield M., Courchesne E., Townsend J. The functional neuroanatomy of spatial attention in autism spectrum disorder. Developmental Neuropsychology 2005, 27:425-458.
37. Haist F., Lee K., Stiles J. Individuating faces and common objects produces equal responses in putative face-processing areas in the ventral occipitotemporal cortex. Frontiers in Human Neuroscience 2010, 4:181.
38. Haxby J.V., Gobbini M.I., Furey M.L., Ishai A., Schouten J.L., Pietrini P. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 2001, 293:2425-2430.
39. Haxby J.V., Hoffman E.A., Gobbini M.I. The distributed human neural system for face perception. Trends in Cognitive Sciences 2000, 4:223-233.
40. Haxby J.V., Hoffman E.A., Gobbini M.I. Human neural systems for face recognition and social communication. Biological Psychiatry 2002, 51:59-67.
41. Ishai A. Let's face it: It's a cortical network. Neuroimage 2008, 40:415-419.
42. Ishai A., Pessoa L., Bikle P.C., Ungerleider L.G. Repetition suppression of faces is modulated by emotion. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:9827-9832.
43. Ishai A., Schmidt C.F., Boesiger P. Face perception is mediated by a distributed cortical network. Brain Research Bulletin 2005, 67:87-93.
44. Johnson M.H. Functional brain development in humans. Nature Reviews: Neuroscience 2001, 2:475-483.
45. Johnson M.H. Interactive specialization: A domain-general framework for human functional brain development?. Developmental Cognitive Neuroscience 2011, 1:7-21.
46. Johnson M.H., Morton J. Biology and cognitive development: The case of face recognition 1991, Blackwell, Oxford, UK & Cambridge, USA.
47. Joseph J.E., Gathers A.D., Bhatt R.S. Progressive and regressive developmental changes in neural substrates for face processing: Testing specific predictions of the interactive specialization account. Developmental Science 2011, 14:227-241.
48. Joseph J.E., Swearingen J.E., Clark J.D., Benca C.E., Collins H.R., Corbly C.R., et al. The changing landscape of functional brain networks for face processing in typical development. Neuroimage 2012, 63:1223-1236.
49. Kanwisher N., McDermott J., Chun M.M. The fusiform face area: A module in human extrastriate cortex specialized for face perception. Journal of Neuroscience 1997, 17:4302-4311.
50. Kanwisher N., Stanley D., Harris A. The fusiform face area is selective for faces not animals. Neuroreport 1999, 10:183-187.
51. Kanwisher N., Yovel G. The fusiform face area: A cortical region specialized for the perception of faces. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 2006, 361:2109-2128.
52. Kaplan J.T., Freedman J., Iacoboni M. Us versus them: Political attitudes and party affiliation influence neural response to faces of presidential candidates. Neuropsychologia 2007, 45:55-64.
53. Keil B., Alagappan V., Mareyam A., McNab J.A., Fujimoto K., Tountcheva V., et al. Size-optimized 32-channel brain arrays for 3T pediatric imaging. Magnetic Resonance in Medicine 2011, 66:1777-1787.
54. Kelly D.J., Quinn P.C., Slater A.M., Lee K., Ge L., Pascalis O. The other-race effect develops during infancy: Evidence of perceptual narrowing. Psychological Science 2007, 18:1084-1089.
55. Kelly D.J., Quinn P.C., Slater A.M., Lee K., Gibson A., Smith M., et al. Three-month-olds, but not newborns, prefer own-race faces. Developmental Science 2005, 8:F31-F36.
56. Kochunov P., Lancaster J., Thompson P., Toga A.W., Brewer P., Hardies J., et al. An optimized individual target brain in the Talairach coordinate system. Neuroimage 2002, 17:922-927.
57. Konrad K., Neufang S., Thiel C.M., Specht K., Hanisch C., Fan J., et al. Development of attentional networks: An fMRI study with children and adults. Neuroimage 2005, 28:429-439.
58. Kouider S., Eger E., Dolan R., Henson R.N. Activity in face-responsive brain regions is modulated by invisible, attended faces: Evidence from masked priming. Cerebral Cortex 2009, 19:13-23.
59. Kriegeskorte N., Formisano E., Sorger B., Goebel R. Individual faces elicit distinct response patterns in human anterior temporal cortex. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:20600-20605.
60. Laird A.R., Robinson J.L., McMillan K.M., Tordesillas-Gutierrez D., Moran S.T., Gonzales S.M., et al. Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: Validation of the Lancaster transform. Neuroimage 2010, 51:677-683.
61. Lancaster J.L., Tordesillas-Gutierrez D., Martinez M., Salinas F., Evans A., Zilles K., et al. Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Human Brain Mapping 2007, 28:1194-1205.
62. Langlois J.H., Ritter J.M., Roggman L.A., Vaughn L.S. Facial diversity and infant preferences for attractive faces. Developmental Psychology 1991, 27:79-84.
63. Lee K., Quinn P.C., Pascalis O., Slater A. Development of face-processing ability in childhood. The Oxford handbook of developmental psychology 2013, Vol. 1: body and mind:338-370. Oxford University Press, New York, NY.
64. Leveroni C.L., Seidenberg M., Mayer A.R., Mead L.A., Binder J.R., Rao S.M. Neural systems underlying the recognition of familiar and newly learned faces. Journal of Neuroscience 2000, 20:878-886.
65. Mazard A., Schiltz C., Rossion B. Recovery from adaptation to facial identity is larger for upright than inverted faces in the human occipito-temporal cortex. Neuropsychologia 2006, 44:912-922.
66. McKone E., Crookes K., Jeffery L., Dilks D.D. A critical review of the development of face recognition: Experience is less important than previously believed. Cognitive Neuropsychology 2012, 29:174-212.
67. Minear M., Park D.C. A lifespan database of adult facial stimuli. Behavior Research Methods, Instruments, & Computers 2004, 36:630-633.
68. Mondloch C.J., Le Grand R., Maurer D. Configural face processing develops more slowly than featural face processing. Perception 2002, 31:553-566.
69. Morris J.P., Pelphrey K.A., McCarthy G. Face processing without awareness in the right fusiform gyrus. Neuropsychologia 2007, 45:3087-3091.
70. Nestor A., Plaut D.C., Behrmann M. Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:9998-10003.
71. Nestor A., Vettel J.M., Tarr M.J. Task-specific codes for face recognition: How they shape the neural representation of features for detection and individuation. PloS One 2008, 3:e3978.
72. Neter J., Kutner M.H., Nachtsheim C.J., Wasserman W. Applied linear statistical models 1996, WCB McGraw-Hill, Boston, MA. 4th ed.
73. Passarotti A.M., Paul B.M., Russiere J.R., Buxton R.B., Wong E.C., Stiles J. The development of face and location processing: An fMRI study. Developmental Science 2003, 6:100-117.
74. Passarotti A.M., Smith J., DeLano M., Huang J. Developmental differences in the neural bases of the face inversion effect show progressive tuning of face-selective regions to the upright orientation. Neuroimage 2007, 34:1708-1722.
75. Peelen M.V., Glaser B., Vuilleumier P., Eliez S. Differential development of selectivity for faces and bodies in the fusiform gyrus. Developmental Science 2009, 12:F16-F25.
76. Pelphrey K.A., Lopez J., Morris J.P. Developmental continuity and change in responses to social and nonsocial categories in human extrastriate visual cortex. Frontiers in Human Neuroscience 2009, 3:25.
77. Perlbarg V., Bellec P., Anton J.L., Pelegrini-Issac M., Doyon J., Benali H. CORSICA: Correction of structured noise in fMRI by automatic identification of ICA components. Magnetic Resonance Imaging 2007, 25:35-46.
78. Phillips P.J., Moon H., Rizvi S.A., Rauss P.J. The FERET evaluation methodology for face-recognition algorithms. IEEE Transactions on Pattern Analysis and Machine Intelligence 2000, 22:1090-1104.
79. Phillips P.J., Wechsler H., Huang J., Rauss P.J. The FERET database and evaluation procedure for face-recognition algorithms. Image and Vision Computing 1998, 16:295-306.
80. Pinsk M.A., Arcaro M., Weiner K.S., Kalkus J.F., Inati S.J., Gross C.G., et al. Neural representations of faces and body parts in macaque and human cortex: A comparative FMRI study. Journal of Neurophysiology 2009, 101:2581-2600.
81. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012, 59:2142-2154.
82. Quinn P.C., Yahr J., Kuhn A., Slater A.M., Pascalis O. Representation of the gender of human faces by infants: A preference for female. Perception 2002, 31:1109-1121.
83. Redcay E., Dodell-Feder D., Pearrow M.J., Mavros P.L., Kleiner M., Gabrieli J.D., et al. Live face-to-face interaction during fMRI: A new tool for social cognitive neuroscience. Neuroimage 2010, 50:1639-1647.
84. Rhodes G., Byatt G., Michie P.T., Puce A. Is the fusiform face area specialized for faces, individuation, or expert individuation?. Journal of Cognitive Neuroscience 2004, 16:189-203.
85. Rolls E.T. The representation of information about faces in the temporal and frontal lobes. Neuropsychologia 2007, 45:124-143.
86. Rossion B., Caldara R., Seghier M., Schuller A.M., Lazeyras F., Mayer E. A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 2003, 126:2381-2395.
87. Scherf K.S., Behrmann M., Humphreys K., Luna B. Visual category-selectivity for faces, places and objects emerges along different developmental trajectories. Developmental Science 2007, 10:F15-F30.
88. Scherf K.S., Luna B., Avidan G., Behrmann M. "What" precedes "which": Developmental neural tuning in face- and place-related cortex. Cerebral Cortex 2011, 21:1963-1980.
89. Schulz K.P., Clerkin S.M., Halperin J.M., Newcorn J.H., Tang C.Y., Fan J. Dissociable neural effects of stimulus valence and preceding context during the inhibition of responses to emotional faces. Human Brain Mapping 2009, 30:2821-2833.
90. Siegel J.S., Power J.D., Dubis J.W., Vogel A.C., Church J.A., Schlaggar B.L., Petersen E. Statistical improvements in functional magnetic resonance imaging analyses produced by censoring high-motion data points. Human Brain Mapping 2013, 10.1002/hbm.22307.
91. Slater A., Bremner G., Johnson S.P., Sherwood P., Hayes R., Brown E. Newborn infants' preference for attractive faces: The role of internal and external facial features. Infancy 2000, 1:265-274.
92. Slater A., Quinn P.C., Hayes R., Brown E. The role of facial orientation in newborn infants' preference for attractive faces. Developmental Science 2000, 3:181-185.
93. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23(1):S208-S219.
94. Somerville L.H., Casey B.J. Developmental neurobiology of cognitive control and motivational systems. Current Opinion in Neurobiology 2010, 20:236-241.
95. Spinoza B.d. Ethics: Demonstrated in geometric order and divided into five parts 1677, Middle Tennessee State University: MTSU Philosophy WebWorks, ([part IV, prop 35, note]) http://frank.mtsu.edu/~rbombard/RB/Spinoza/ethica-front.html.
96. Stevens M.C., Pearlson G.D., Calhoun V.D. Changes in the interaction of resting-state neural networks from adolescence to adulthood. Human Brain Mapping 2009, 30:2356-2366.
97. Supekar K., Uddin L.Q., Prater K., Amin H., Greicius M.D., Menon V. Development of functional and structural connectivity within the default mode network in young children. Neuroimage 2010, 52:290-301.
98. Talairach J., Tournoux P. Co-planar stereotaxic atlas of the human brain 1988, Thieme Medical, New York.
99. Taylor M.J., Batty M., Itier R.J. The faces of development: A review of early face processing over childhood. Journal of Cognitive Neuroscience 2004, 16:1426-1442.
100. Thomas M.S., Annaz D., Ansari D., Scerif G., Jarrold C., Karmiloff-Smith A. Using developmental trajectories to understand developmental disorders. Journal of Speech Language and Hearing Research 2009, 52:336-358.
101. Tregellas J.R., Tanabe J.L., Miller D.E., Freedman R. Monitoring eye movements during fMRI tasks with echo planar images. Human Brain Mapping 2002, 17:237-243.
102. Tsao D.Y., Livingstone M.S. Mechanisms of face perception. Annual Review of Neuroscience 2008, 31:411-437.
103. Turati C., Simion F., Milani I., Umiltà C. Newborns' preference for faces: What is crucial?. Developmental Psychology 2002, 38:875-882.
104. Van Dijk K.R., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 2012, 59:431-438.
105. Want S.C., Pascalis O., Coleman M., Blades M. Recognizing people from the inner or outer parts of their faces: Developmental data concerning 'unfamiliar' faces. British Journal of Developmental Psychology 2003, 21:125-135.
106. Wechsler D. Wechsler abbreviated scale of intelligence manual 1999, The Psychological Corporation, New York.
107. Weiner K.S., Grill-Spector K. The improbable simplicity of the fusiform face area. Trends in Cognitive Sciences 2012, 16:251-254.
108. Willenbockel V., Sadr J., Fiset D., Horne G., Gosselin F.d.r., Tanaka J. The SHINE toolbox for controlling low-level image properties. Journal of Vision 2010, 10:653.
109. Wojciulik E., Kanwisher N., Driver J. Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. Journal of Neurophysiology 1998, 79:1574-1578.
110. Xu Y. Revisiting the role of the fusiform face area in visual expertise. Cerebral Cortex 2005, 15:1234-1242.
111. Yovel G., Kanwisher N. Face perception: Domain specific, not process specific. Neuron 2004, 44:889-898.
112. Yovel G., Kanwisher N. The neural basis of the behavioral face-inversion effect. Current Biology 2005, 15:2256-2262.