Holistic face categorization in higher order visual areas of the normal and prosopagnosic brain: toward a non-hierarchical view of face perception.
How a visual stimulus is initially categorized as a face in a network of human brain areas remains largely unclear. Hierarchical neuro-computational models of face perception assume that the visual stimulus is first decomposed in local parts in lower order visual areas. These parts would then be combined into a global representation in higher order face-sensitive areas of the occipito-temporal cortex. Here we tested this view in fMRI with visual stimuli that are categorized as faces based on their global configuration rather than their local parts (two-tones Mooney figures and Arcimboldo's facelike paintings). Compared to the same inverted visual stimuli that are not categorized as faces, these stimuli activated the right middle fusiform gyrus ("Fusiform face area") and superior temporal sulcus (pSTS), with no significant activation in the posteriorly located inferior occipital gyrus (i.e., no "occipital face area"). This observation is strengthened by behavioral and neural evidence for normal face categorization of these stimuli in a brain-damaged prosopagnosic patient whose intact right middle fusiform gyrus and superior temporal sulcus are devoid of any potential face-sensitive inputs from the lesioned right inferior occipital cortex. Together, these observations indicate that face-preferential activation may emerge in higher order visual areas of the right hemisphere without any face-preferential inputs from lower order visual areas, supporting a non-hierarchical view of face perception in the visual cortex.
Institute of Research in Psychology, University of Louvain Louvain-la-Neuve, Belgium.
Bruno
B
Rossion
Laurence
L
Dricot
Rainer
R
Goebel
Thomas
T
Busigny
J Cogn Neurosci. 1996 Summer;8(3):197-230
23968149
J Exp Psychol Hum Percept Perform. 2004 Feb;30(1):104-18
14769071
Vision Res. 1998 Aug;38(15-16):2429-54
9798008
J Neurophysiol. 2010 Mar;103(3):1501-7
20071627
J Neurosci. 2010 Mar 3;30(9):3544-52
20203214
Curr Biol. 2007 Sep 18;17(18):1568-73
17764942
Nat Neurosci. 2001 May;4(5):533-9
11319563
J Vis. 2010 Feb 26;10(2):25.1-16
20462326
J Opt Soc Am A. 1987 Oct;4(10):2006-21
3430211
Percept Mot Skills. 1970 Oct;31(2):491-8
5492324
Hum Brain Mapp. 1999;7(1):29-37
9882088
J Cogn Neurosci. 2005 Oct;17(10):1652-66
16269103
Trends Cogn Sci. 2007 Feb;11(2):58-64
17188555
Perception. 2004;33(8):939-56
15521693
Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19514-9
19033466
J Neurosci. 2009 Jun 17;29(24):7788-96
19535590
Neuroimage. 2006 Sep;32(3):1243-9
16861009
J Cogn Neurosci. 1996 Nov;8(6):551-565
20740065
Curr Biol. 2005 Dec 20;15(24):2256-62
16360687
Brain. 2003 Sep;126(Pt 9):2093-107
12821517
J Cogn Neurosci. 2008 May;20(5):863-78
18201134
Can J Psychol. 1956 Dec;10(4):191-9
13374609
Cognition. 1998 Aug;68(1):B1-11
9775518
J Vis. 2007 Jan 31;7(1):10
17461678
J Cogn Neurosci. 2005 Apr;17(4):580-90
15829079
Can J Psychol. 1957 Dec;11(4):219-26
13489559
Hum Neurobiol. 1984;3(4):197-208
6526706
Neuropsychologia. 2010 Jul;48(9):2620-9
20457169
Brain Res Cogn Brain Res. 2003 Jul;17(2):431-46
12880913
Cereb Cortex. 1991 Jan-Feb;1(1):1-47
1822724
Brain. 2003 Nov;126(Pt 11):2381-95
12876150
Exp Brain Res. 1989;78(1):193-202
2591512
Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):17083-8
12477930
Neuropsychologia. 2002;40(8):1196-208
11931923
Curr Biol. 2007 Jan 9;17(1):R7-8
17208177
Behav Brain Res. 1988 Aug;29(3):245-58
3139010
Trends Cogn Sci. 2000 Jun;4(6):223-233
10827445
Neuroreport. 1997 Apr 14;8(6):1417-23
9172146
J Cogn Neurosci. 2003 Apr 1;15(3):419-31
12729493
Cereb Cortex. 2007 Mar;17(3):669-78
16648454
Psychol Bull. 1957 May;54(3):197-217
13441847
Neuron. 2006 Apr 6;50(1):159-72
16600863
Prog Brain Res. 2001;134:193-204
11702544
Hum Brain Mapp. 2009 May;30(5):1637-51
18661501
Brain Cogn. 1989 Jul;10(2):149-70
2757824
Cognition. 1998 Jul;67(1-2):45-71
9735536
J Cogn Neurosci. 2000 May;12(3):495-504
10931774
Neuroimage. 2007 Apr 1;35(2):836-52
17303440
Acta Psychol (Amst). 2001 Apr;107(1-3):293-321
11388140
J Physiol. 1962 Jan;160:106-54
14449617
Nature. 1999 Aug 26;400(6747):869-73
10476965
Brain. 1989 Aug;112 ( Pt 4):975-95
2775997
J Neurosci. 1996 Jul 1;16(13):4207-21
8753882
Neuroimage. 2003 Sep;20(1):520-8
14527612
Nature. 1998 Aug 20;394(6695):784-7
9723617
Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8135-9
7667258
Proc R Soc Lond B Biol Sci. 1982 Mar 22;214(1197):501-24
6127693
Cortex. 2003 Jun;39(3):533-40
12870826
J Cogn Neurosci. 2007 Nov;19(11):1735-52
17958478
J Neurol Sci. 1972 Feb;15(2):167-72
5010102
Cortex. 2010 Sep;46(8):965-81
19683710
Nature. 1998 Oct 29;395(6705):852-3
9804417
Neuropsychologia. 2006;44(4):594-609
16125741
J Clin Exp Neuropsychol. 1998 Oct;20(5):755-62
10079050
Arch Neurol. 1962 Aug;7:92-100
13905818
Psychol Rev. 1987 Apr;94(2):115-147
3575582
Curr Biol. 2005 Jun 7;15(11):993-1005
15936269
Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):15164-9
12417754
Nature. 1999 Feb 4;397(6718):430-3
9989408
J Cogn Neurosci. 1997 Fall;9(5):605-10
23965119
Nature. 1997 Oct 9;389(6651):596-9
9335498
Nature. 2009 Jul 2;460(7251):94-7
19506558
Cereb Cortex. 2007 Feb;17(2):325-38
16525131
J Neurosci. 1997 Jun 1;17(11):4302-11
9151747
Neuroimage. 2006 Sep;32(3):1385-94
16870475
Brain. 1988 Dec;111 ( Pt 6):1287-97
3208058
Biol Cybern. 1992;66(3):241-51
1540675
Neuropsychologia. 2010 Mar;48(4):933-44
19944710
Neuropsychologia. 2002;40(13):2305-13
12417460
Brain. 1972;95(1):61-78
5023091
Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20600-5
18077383
Trends Neurosci. 2000 Nov;23(11):571-9
11074267
Cereb Cortex. 2011 Feb;21(2):467-76
20576927
Cereb Cortex. 2001 Apr;11(4):287-97
11278192
Science. 2001 Sep 28;293(5539):2425-30
11577229
Nat Neurosci. 1999 Nov;2(11):1019-25
10526343
J Cogn Neurosci. 2003 May 15;15(4):600-9
12803970
Neuroimage. 2008 Apr 1;40(2):423-426
18086537
J Neurosci. 1998 Mar 15;18(6):2188-99
9482803
J Neurosci. 1993 Sep;13(9):3681-91
7690064
Perception. 2003;32(8):903-20
14580138
Neuroimage. 2010 Oct 1;52(4):1559-73
20457261
Neuroimage. 2008 Apr 1;40(2):415-419
18063389
Neuropsychologia. 1990;28(11):1143-61
2290490
Neuron. 2002 Dec 5;36(5):791-804
12467584
Cortex. 1987 Mar;23(1):99-110
3568709
J Cogn Neurosci. 1997 Fall;9(5):555-604
23965118
Neuropsychologia. 2009 Nov;47(13):2798-811
19524599
Neuropsychologia. 1971 Mar;9(1):97-113
5146491
J Neurosci. 1984 Aug;4(8):2051-62
6470767
J Cogn Neurosci. 2001 Aug 15;13(6):744-53
11564319
Neurology. 2002 Jan 8;58(1):71-8
11781408
Cereb Cortex. 2006 Feb;16(2):183-91
15858161
Brain. 1992 Feb;115 Pt 1:15-36
1559150
J Exp Psychol Learn Mem Cogn. 2004 Jan;30(1):181-97
14736306
PLoS One. 2008;3(12):e3978
19112516
Cereb Cortex. 2006 Apr;16(4):574-86
16033923
Cereb Cortex. 1992 Sep-Oct;2(5):389-400
1422093
J Vis. 2003;3(6):440-55
12901715
Hum Brain Mapp. 1998;6(4):316-28
9704268
Cereb Cortex. 2007 Oct;17(10):2400-6
17190969
Brain Cogn. 1990 Sep;14(1):1-18
2223040
J Neuropsychol. 2008 Mar;2(1):245-68
19334313
J Cogn Neurosci. 2001 Jul 1;13(5):556-76
11506657
Neuroimage. 2004 Jan;21(1):91-8
14741646
Nat Neurosci. 2001 Aug;4(8):832-8
11477430
Neuroimage. 2008 Mar 1;40(1):318-32
18164628
J Vis. 2010 Apr 28;10(4):16.1-17
20465335
Neuropsychologia. 2010 Jun;48(7):2051-67
20362595
Arch Psychiatr Nervenkr Z Gesamte Neurol Psychiatr. 1947;118(1-2):6-53
18901747
Cereb Cortex. 1992 Sep-Oct;2(5):375-88
1422092
Soc Cogn Affect Neurosci. 2009 Mar;4(1):101-9
19151374
J Cogn Neurosci. 1991 Winter;3(1):42-58
23964804
Nat Neurosci. 2009 Jan;12(1):29-31
19029889
Neuron. 1993 Feb;10(2):115-25
8094962