Development of face discrimination abilities, and relationship to magnocellular pathway development, between childhood and adulthood

Visual Neuroscience

Volumn 30, Issue 5-6, 2013, Pages 251-262

  Pallett, Pamela M ^a   Dobkins, Karen R ^b  

^a Ohio State University   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Development; Face perception; Face processing; linking hypotheses; Magnocellular; Object processing; Parvocellular; Vision

Indexed keywords

ADOLESCENT; ADULT; AGE DISTRIBUTION; ARTICLE; CHILD; FACE; FACE DEVELOPMENT; FACE DISCRIMINATION; FEMALE; HUMAN; HUMAN EXPERIMENT; LUMINANCE; MALE; NORMAL HUMAN; PEDIATRICS; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; YOUNG ADULT;

ADOLESCENT; ADULT; CHILD; CONTRAST SENSITIVITY; DISCRIMINATION (PSYCHOLOGY); FACE; FEMALE; HUMAN DEVELOPMENT; HUMANS; MALE; VISUAL PATHWAYS; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84893538131     PISSN: 09525238     EISSN: 14698714     Source Type: Journal    
DOI: 10.1017/S0952523813000217     Document Type: Article

References (109)

1. ADOLPHS, R., BARON-COHEN, S. & TRANEL, D. (2002). Impaired recognition of social emotions following amygdala damage. Journal of Cognitive Neuroscience 14, 1264-1274.
2. ADOLPHS, R., GOSSELIN, F., BUCHANAN, T.W., TRANEL, D., SCHYNS, P. & DAMASIO, A.R. (2005). A mechanism for impaired fear recognition after amygdala damage. Nature 433, 68-72.
3. BAR, M. (2003). A cortical mechanism for triggering top-down facilitation in visual object recognition. Journal of Cognitive Neuroscience 15, 600-609.
4. BARBAS, H. (1995). Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neuroscience and Biobehavioral Reviews 19, 499-510.
5. BEAZLEY, L.D., ILLINGWORTH, D.J., JAHN, A. & GREER, D.V. (1980). Contrast sensitivity in children and adults. The British Journal of Ophthalmology 64, 863-866.
6. BENEDEK, G., BENEDEK, K., KERI, S. & JANAKY, M. (2003). The scotopic low-frequency spatial contrast sensitivity develops in children between the ages of 5 and 14 years. Neuroscience Letters 345, 161-164.
7. BOON, M.Y., SUTTLE, C.M., HENRY, B.I. & DAIN, S.J. (2009). Dynamics of chromatic visual system processing differ in complexity between children and adults. Journal of Vision 9, 1-17.
8. BOSWORTH, R.G. & DOBKINS, K.R. (2009). Chromatic and luminance contrast sensitivity in fullterm and preterm infants. Journal of Vision 9, 11-16.
9. BRACE, N.A., HOLE, G.J., KEMP, R.I., PIKE, G.E., VAN DUUREN, M. & NORGATE, L. (2001). Developmental changes in the effect of inversion: Using a picture book to investigate face recognition. Perception 30, 85-94.
10. BRAINARD, D.H. (1997). The psychophysics toolbox. Spatial Vision 10, 433-436.
11. BULLIER, J. & NOWAK, L.G. (1995). Parallel versus serial processing: New vistas on the distributed organization of the visual system. Current Opinion in Neurobiology 5, 497-503.
12. CAREY, S. & DIAMOND, R. (1977). From piecemeal to configurational representation of faces. Science 195, 312-314.
13. CAREY, S., DIAMOND, R. & WOODS, B. (1980). Development of face recognition: A maturational component? Developmental Psychology 16, 4, 257-269.
14. CAVADA, C., COMPANY, T., TEJEDOR, J., CRUZ-RIZZOLO, R.J. & REINOSO-SUAREZ, F. (2000). The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cerebral Cortex 10, 220-242.
15. CHEN, C.M., LAKATOS, P., SHAH, A.S., MEHTA, A.D., GIVRE, S.J., JAVITT, D.C. & SCHROEDER, C.E. (2007). Functional anatomy and interaction of fast and slow visual pathways in macaque monkeys. Cerebral Cortex 17, 1561-1569.
16. CROGNALE, M.A. (2002). Development, maturation, and aging of chromatic visual pathways: VEP results. Journal of Vision 2, 438-450.
17. CROOKES, K. & MCKONE, E. (2009). Early maturity of face recognition: No childhood development of holistic processing, novel face encoding, or face-space. Cognition 111, 219-247.
18. DE HEERING, A., ROSSION, B. & MAURER, D. (2012). Developmental changes in face recognition during childhood: Evidence from upright and inverted faces. Cognitive Development 27, 17-27.
19. DELORME, A. & THORPE, S.J. (2001). Face identification using one spike per neuron: Resistance to image degradations. Neural Networks: The Official Journal of the International Neural Network Society 14, 795-803.
20. DERUELLE, C., RONDAN, C., GEPNER, B. & TARDIF, C. (2004). Spatial frequency and face processing in children with autism and Asperger syndrome. Journal of Autism and Developmental Disorders 34, 199-210.
21. DIAMOND, R. & CAREY, S. (1977). Developmental changes in the representation of faces. Journal of Experimental Child Psychology 23, 1-22.
22. DOBKINS, K.R., ANDERSON, C.M. & LIA, B. (1999). Infant temporal contrast sensitivity functions (tCSFs) mature earlier for luminance than for chromatic stimuli: Evidence for precocious magnocellular development? Vision Research 39, 3223-3239.
23. DOBKINS, K.R., BOSWORTH, R.G. & MCCLEERY, J.P. (2009). Effects of ges-tational length, gender, postnatal age, and birth order on visual contrast sensitivity in infants. Journal of Vision 9, 11-21.
24. DOBKINS, K.R. & TELLER, D.Y. (1996a). Infant contrast detectors are selective for direction of motion. Vision Research 36, 281-294.
25. DOBKINS, K.R. & TELLER, D.Y. (1996b). Infant motion: Detection (M:D) ratios for chromatically defined and luminance-defined moving stimuli. Vision Research 36, 3293-3310.
26. FARRONI, T., JOHNSON, M.H., MENON, E., ZULIAN, L., FARAGUNA, D. & CSIBRA, G. (2005). Newborns' preference for face-relevant stimuli: Effects of contrast polarity. Proceedings of the National Academy of Sciences of the United States of America 102, 17245-17250.
27. FIORENTINI, A., MAFFEI, L. & SANDINI, G. (1983). The role of high spatial frequencies in face perception. Perception 12, 195-201.
28. FREIRE, A., LEE, K. & SYMONS, L.A. (2000). The face-inversion effect as a deficit in the encoding of configural information: Direct evidence. Perception 29, 159-170.
29. GARRIDO, M.I., BARNES, G.R., SAHANI, M. & DOLAN, R.J. (2012). Functional evidence for a dual route to amygdala. Current Biology: CB 22, 129-134.
30. GAUTHIER, I., BEHRMANN, M. & TARR, M.J. (1999). Can face recognition really be dissociated from object recognition? Journal of Cognitive Neuroscience 11, 349-370.
31. GAUTHIER, I., BEHRMANN, M. & TARR, M.J. (2004). Are Greebles like faces? Using the neuropsychological exception to test the rule. Neuropsychologia 42, 1961-1970.
32. GERMINE, L.T., DUCHAINE, B. & NAKAYAMA, K. (2011). Where cognitive development and aging meet: Face learning ability peaks after age 30. Cognition 118, 201-210.
33. GHASHGHAEI, H.T., HILGETAG, C.C. & BARBAS, H. (2007). Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. NeuroImage 34, 905-923.
34. GOFFAUX, V. & ROSSION, B. (2007). Face inversion disproportionately impairs the perception of vertical but not horizontal relations between features. Journal of Experimental Psychology: Human Perception and Performance 33, 995-1001.
35. GOLARAI, G., GHAHREMANI, D.G., WHITFIELD-GABRIELI, S., REISS, A., EBERHARDT, J.L., GABRIELI, J.D.E. & GRILL-SPECTOR, K. (2007). Differential development of high-level visual cortex correlates with category-specific recognition memory. Nature Neuroscience 10, 512-522.
36. GOLARAI, G., LIBERMAN, A., YOON, J.M. & GRILL-SPECTOR, K. (2010). Differential development of the ventral visual cortex extends through adolescence. Frontiers in Human Neuroscience 3, 80.
37. GRILL-SPECTOR, K., KUSHNIR, T., EDELMAN, S., AVIDAN, G., ITZCHAK, Y. & MALACH, R. (1999). Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24, 187-203.
38. GUNTHER, K.L. & DOBKINS, K.R. (2002). Individual differences in chromatic (red/green) contrast sensitivity are constrained by the relative number of L-versus M-cones in the eye. Vision Research 42, 1367-1378.
39. JEFFERY, L., MCKONE, E., HAYNES, R., FIRTH, E., PELLICANO, E. & RHODES, G. (2010). Four-to-six-year-old children use norm-based coding in face-space. Journal of Vision 10, 18.
40. JOHNSON, M.H. (2005). Subcortical face processing. Nature Reviews Neuroscience 6, 766-774.
41. JOHNSON, M.H. (2011). Face processing as a brain adaptation at multiple timescales. Quarterly Journal of Experimental Psychology 64, 1873-1888.
42. JONES, E.G. & BURTON, H. (1976). A projection from the medial pulvinar to the amygdala in primates. Brain Research 104, 142-147.
43. KANWISHER, N., MCDERMOTT, J. & CHUN, M.M. (1997). The fusiform face area: A module in human extrastriate cortex specialized for face perception. Journal of Neuroscience 17, 4302-4311.
44. KANWISHER, N., TONG, F. & NAKAYAMA, K. (1998). The effect of face inversion on the human fusiform face area. Cognition 68, B1-B11.
45. KNOBLAUCH, K., VITAL-DURAND, F. & BARBUR, J.L. (2001). Variation of chromatic sensitivity across the life span. Vision Research 41, 23-36.
46. KROLAK-SALMON, P., HENAFF, M.A., VIGHETTO, A., BERTRAND, O. & MAUGUIERE, F. (2004). Early amygdala reaction to fear spreading in occipital, temporal, and frontal cortex: A depth electrode ERP study in human. Neuron 42, 665-676.
47. KVERAGA, K., BOSHYAN, J. & BAR, M. (2007). Magnocellular projections as the trigger of top-down facilitation in recognition. Journal of Neuroscience 27, 13232-13240.
48. LANGNER, O., DOTSCH, R., BIJLSTRA, G., WIGBOLDUS, D.H.J., HAWK, S.T. & VAN KNIPPENBERG, A. (2010). Presentation and validation of the Radboud Faces Database. Cognition & Emotion 24, 1377-1388.
49. LENNIE, P. & D'ZMURA, M. (1988). Mechanisms of color vision. Critical Reviews in Neurobiology 3, 333-400.
50. LINDSEY, D.T. & TELLER, D.Y. (1990). Motion at isoluminance: Discrimination/detection ratios for moving isoluminant gratings. Vision Research 30, 1751-1761.
51. LINKE, R., DE LIMA, A.D., SCHWEGLER, H. & PAPE, H.C. (1999). Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: Possible substrates of a subcortical visual pathway to the amygdala. The Journal of Comparative Neurology 403, 158-170.
52. LUNDY, B.A., JACKSON, J.W. & HAAF, R.A. (2001). Stimulus properties, attentional limitations, and young children's face recognition. Perceptual and Motor Skills 92, 919-929.
53. MACCHI CASSIA, V., PICOZZI, M., KUEFNER, D., BRICOLO, E. & TURATI, C. (2009). Holistic processing for faces and cars in preschool-aged children and adults: Evidence from the composite effect. Developmental Science 12, 236-248.
54. MACCHI CASSIA, V., TURATI, C. & SCHWARZER, G. (2011). Sensitivity to spacing changes in faces and nonface objects in preschool-aged children and adults. Journal of Experimental Child Psychology 109, 454-467.
55. MAUNSELL, J.H., NEALEY, T.A. & DEPRIEST, D.D. (1990). Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 10, 3323-3334.
56. MCKONE, E. & BOYER, B.L. (2006). Sensitivity of 4-year-olds to featural and second-order relational changes in face distinctiveness. Journal of Experimental Child Psychology 94, 134-162.
57. MCKONE, E., CROOKES, K., JEFFERY, L. & DILKS, D.D. (2012). A critical review of the development of face recognition: Experience is less important than previously believed. Cognitive Neuropsychology 29, 174-212.
58. MCKONE, E., CROOKES, K. & KANWISHER, N. (2009). The cognitive and neural development of face recognition in humans. In The Cognitive Neurosciences, ed. GAZZANIGA, M.S. (4th ed), pp. 467-482. Cambridge, MA: MIT Press.
59. MERIGAN, W.H. & ESKIN, T.A. (1986). Spatio-temporal vision of macaques with severe loss of P beta retinal ganglion cells. Vision Research 26, 1751-1761.
60. MERIGAN, W.H., KATZ, L.M. & MAUNSELL, J.H. (1991). The effects of parvocellular lateral geniculate lesions on the acuity and contrast sensitivity of macaque monkeys. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 11, 994-1001.
61. MERIGAN, W.H. & MAUNSELL, J.H. (1990). Macaque vision after magno-cellular lateral geniculate lesions. Visual Neuroscience 5, 347-352.
62. MERIGAN, W.H. & MAUNSELL, J.H. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience 16, 369-402.
63. MONDLOCH, C.J., LE GRAND, R. & MAURER, D. (2002). Configural face processing develops more slowly than featural face processing. Perception 31, 553-566.
64. MONDLOCH, C.J., MAURER, D. & AHOLA, S. (2006). Becoming a face expert. Psychological Science 17, 930-934.
65. MONDLOCH, C.J., PATHMAN, T., MAURER, D., LE GRAND, R. & DE SCHONEN, S. (2007). The composite face effect in six-year-old children: Evidence of adult-like holistic face processing. Visual Cognition 15, 564-577.
66. MORRIS, J.S., DEGELDER, B., WEISKRANTZ, L. & DOLAN, R.J. (2001). Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain: A Journal of Neurology 124, 1241-1252.
67. MORRIS, J.S., OHMAN, A. & DOLAN, R.J. (1999). A subcortical pathway to the right amygdala mediating "unseen" fear. Proceedings of the National Academy of Sciences of the United States of America 96, 1680-1685.
68. PASCALIS, O., DE VIVIES, X.D., ANZURES, G., QUINN, P.C., SLATER, A.M., TANAKA, J.W. & LEE, K. (2011). Development of face processing. Wiley Interdisciplinary Reviews. Cognitive Science 2, 666-675.
69. PASLEY, B.N., MAYES, L.C. & SCHULTZ, R.T. (2004). Subcortical discrimination of unperceived objects during binocular rivalry. Neuron 42, 163-172.
70. PASSAROTTI, A.M., PAUL, B.M., BUSSIER, J.R., BUXTON, R.B., WONG, E.C. & STILES, J. (2003). The development of face and location processing: An fMRI study. Developmental Science 6, 100-117.
71. PEELEN, M.V., GLASER, B., VUILLEUMIER, P. & ELIEZ, S. (2009). Differential development of selectivity for faces and bodies in the fusiform gyrus. Developmental Science 12, F16-F25.
72. PELLI, D.G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision 10, 437-442.
73. PELLICANO, E. & RHODES, G. (2003). Holistic processing of faces in preschool children and adults. Psychological Science 14, 618-622.
74. PELLICANO, E., RHODES, G. & PETERS, M. (2006). Are preschoolers sensitive to configural information in faces? Developmental Science 9, 270-277.
75. PESSOA, L. & ADOLPHS, R. (2010). Emotion processing and the amygdala: From a 'low road' to 'many roads' of evaluating biological significance. Nature Reviews Neuroscience 11, 773-783.
76. PICOZZI, M., CASSIA, V.M., TURATI, C. & VESCOVO, E. (2009). The effect of inversion on 3-to 5-year-olds' recognition of face and nonface visual objects. Journal of Experimental Child Psychology 102, 487-502.
77. PITCHER, D., CHARLES, L., DEVLIN, J.T., WALSH, V. & DUCHAINE, B. (2009). Triple dissociation of faces, bodies, and objects in extrastriate cortex. Current Biology: CB 19, 319-324.
78. REMPEL-CLOWER, N.L. & BARBAS, H. (2000). The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. Cerebral Cortex 10, 851-865.
79. RICHLER, J.J., MACK, M.L., PALMERI, T.J. & GAUTHIER, I. (2011). Inverted faces are (eventually) processed holistically. Vision Research 51, 333-342.
80. ROLLS, E.T., COWEY, A. & BRUCE, V. (1992). Neurophysiological mechanisms underlying face processing within and beyond the temporal cortical visual areas. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 335, 11-21.
81. ROMANSKI, L.M., GIGUERE, M., BATES, J.F. & GOLDMAN-RAKIC, P.S. (1997). Topographic organization of medial pulvinar connections with the prefrontal cortex in the rhesus monkey. The Journal of Comparative Neurology 379, 313-332.
82. ROSSION, B. (2008). Picture-plane inversion leads to qualitative changes of face perception. Acta Psychologica 128, 274-289.
83. ROTSHTEIN, P., GENG, J.J., DRIVER, J. & DOLAN, R.J. (2007). Role of features and second-order spatial relations in face discrimination, face recognition, and individual face skills: Behavioral and functional magnetic resonance imaging data. Journal of Cognitive Neuroscience 19, 1435-1452.
84. SANGRIGOLI, S. & DE SCHONEN, S. (2004). Effect of visual experience on face processing: A developmental study of inversion and non-native effects. Developmental Science 7, 74-87.
85. SCHERF, K.S., BEHRMANN, M., HUMPHREYS, K. & LUNA, B. (2007). Visual category-selectivity for faces, places and objects emerges along different developmental trajectories. Developmental Science 10, F15-30.
86. SCHILLER, P.H., LOGOTHETIS, N.K. & CHARLES, E.R. (1990). Functions of the colour-opponent and broad-band channels of the visual system. Nature 343, 68-70.
87. SCHILLER, P.H., MALPELI, J.G. & SCHEIN, S.J. (1979). Composition of geniculostriate input to superior colliculus of the rhesus monkey. Journal of Neurophysiology 42, 1124-1133.
88. SEARCY, J.H. & BARTLETT, J.C. (1996). Inversion and processing of component and spatial-relational information in faces. Journal of Experimental Psychology. Human Perception and Performance 22, 904-915.
89. SEKULER, A.B., GASPAR, C.M., GOLD, J.M. & BENNETT, P.J. (2004). Inversion leads to quantitative, not qualitative, changes in face processing. Current Biology: CB 14, 391-396.
90. SERGENT, J. (1985). Influence of task and input factors on hemispheric involvement in face processing. Journal of Experimental Psychology: Human Perception and Performance, 11, 6, 846-861.
91. SHAPLEY, R. (1990). Visual sensitivity and parallel retinocortical channels. Annual Review of Psychology 41, 635-658.
92. SHORT, L.A., HATRY, A.J. & MONDLOCH, C.J. (2011). The development of norm-based coding and race-specific face prototypes: An examination of 5-and 8-year-olds' face space. Journal of Experimental Child Psychology 108, 338-357.
93. SKOTTUN, B.C. (2000). The magnocellular deficit theory of dyslexia: The evidence from contrast sensitivity. Vision Research 40, 111-127.
94. SPEZIO, M.L., HUANG, P.Y., CASTELLI, F. & ADOLPHS, R. (2007). Amygdala damage impairs eye contact during conversations with real people. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 27, 3994-3997.
95. TANAKA, J.W. & CORNEILLE, O. (2007). Typicality effects in face and object perception: Further evidence for the attractor field model. Perception & Psychophysics 69, 619-627.
96. TANAKA, J.W. & FARAH, M.J. (1993). Parts and wholes in face recognition. Quarterly Journal of Experimental Psychology. A-Human Experimental Psychology 46, 225-245.
97. TANAKA, J.W., MEIXNER, T.L. & KANTNER, J. (2011). Exploring the perceptual spaces of faces, cars and birds in children and adults. Developmental Science 14, 762-768.
98. TAYLOR, M.M. & CREELMAN, C.D. (1967). PEST: Efficiency estimates on probability functions. Journal of the Acoustical Society of America 41, 782-787.
99. TAYLOR, M.J., MCCARTHY, G., SALIBA, E. & DEGIOVANNI, E. (1999). ERP evidence of developmental changes in processing of faces. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 110, 910-915.
100. TELLER, D. (1982). Scotopic vision, color vision, and stereopsis in infants. Current Eye Research 2, 199-210.
101. TELLER, D. (1984). Linking propositions. Vision Research 24, 1233-1246.
102. TILL, C., WESTALL, C.A., KOREN, G., NULMAN, I. & ROVET, J.F. (2005). Vision abnormalities in young children exposed prenatally to organic solvents. Neurotoxicology 26, 599-613.
103. VALENTINE, T. (1988). Upside-down faces: A review of the effect of inversion upon face recognition. British Journal of Psychology 79, 471-491.
104. VUILLEUMIER, P., ARMONY, J.L., DRIVER, J. & DOLAN, R.J. (2003). Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nature Neuroscience 6, 624-631.
105. WHALEN, P.J., RAUCH, S.L., ETCOFF, N.L., MCINERNEY, S.C., LEE, M.B. & JENIKE, M.A. (1998). Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 18, 411-418.
106. WICHMANN, F.A. & HILL, N.J. (2001). The psychometric function: I. Fitting, sampling and goodness-of-fit. Perception & Psychophysics 63, 1293-1313.
107. WINSTON, J.S., VUILLEUMIER, P. & DOLAN, R.J. (2003). Effects of low-spatial frequency components of fearful faces on fusiform cortex activity. Current Biology: CB 13, 1824-1829.
108. YAMASHITA, J.A, HARDY, J.L., DE VALOIS, K.K. & WEBSTER, M.A. (2005). Stimulus selectivity of figural aftereffects for faces. Journal of Experimen tal Psychology. Human Perception and Performance 31, 420-437.
109. ZHAO, L. & CHUBB, C. (2001). The size-tuning of the face-distortion aftereffect. Vision Research 41, 2979-2994.