Congenital prosopagnosia: Multistage anatomical and functional deficits in face processing circuitry

Journal of Neurology

Volumn 258, Issue 5, 2011, Pages 770-782

  Dinkelacker, V ^a,b   Gruter M ^c,d,f   Klaver, P ^a,e   Gruter T ^a   Specht, K ^g   Weis, S ^h   Kennerknecht, I ^c   Elger, C E ^a   Fernandez, G ^a,i  

^a UNIVERSITY OF BONN   (Germany)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d Nottulner Landweg   (Germany)

^e UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^f UNIVERSITY OF BAMBERG   (Germany)

^g HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^h DURHAM UNIVERSITY   (United Kingdom)

ⁱ RADBOUD UNIVERSITY   (Netherlands)

Author keywords

Congenital prosopagnosia; Emotion; Functional MRI; Fusiform gyrus; Voxel based morphometry

Indexed keywords

ADULT; ANATOMICAL VARIATION; ARTICLE; BEHAVIOR; CLINICAL ARTICLE; CONGENITAL PROSOPAGNOSIA; CONTROLLED STUDY; DENSITY; EMOTION; FACE PROFILE; FACE RECOGNITION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; GRAY MATTER; HUMAN; LINGUAL GYRUS; LONG TERM MEMORY; MALE; MIDDLE TEMPORAL GYRUS; NERVE CELL MEMBRANE POTENTIAL; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROSOPAGNOSIA; VISION; VISUAL INFORMATION; VISUAL MEMORY; VISUAL STIMULATION; VOXEL BASED MORPHOMETRY;

ADULT; BRAIN MAPPING; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, LONG-TERM; PATTERN RECOGNITION, VISUAL; PROSOPAGNOSIA;

EID: 79960004107     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-010-5828-5     Document Type: Article

References (67)

1. Bouvier SE, Engel SA (2006) Behavioral deficits and cortical damage loci in cerebral achromatopsia. Cereb Cortex 16:183-191 (Pubitemid 43100063)
2. Damasio AR, Damasio H, Van Hoesen GW (1982) Prosopagnosia: anatomic basis and behavioral mechanisms. Neurology 32:331-341 (Pubitemid 12144271)
3. Kennerknecht I, Grueter T, Welling B, Wentzek S, Horst J et al (2006) First report of prevalence of non-syndromic hereditary prosopagnosia (HPA). Am J Med Genet A 140:1617-1622 (Pubitemid 44148246)
4. Kennerknecht I, Ho NY, Wong VC (2008) Prevalence of hereditary prosopagnosia (HPA) in Hong Kong Chinese population. Am J Med Genet A 146 A: 2863-2870
5. Kennerknecht I, Pluempe N, Welling B (2008) Congenital prosopagnosia-a common hereditary cognitive dysfunction in humans. Front Biosci 13:3150-3158 (Pubitemid 351589226)
6. Kennerknecht I, Plumpe N, Edwards S, Raman R (2007) Hereditary prosopagnosia (HPA): the first report outside the Caucasian population. J Hum Genet 52:230-236
7. Behrmann M, Avidan G (2005) Congenital prosopagnosia: faceblind from birth. Trends Cogn Sci 9:180-187
8. Thomas C, Avidan G, Humphreys K, Jung KJ, Gao F et al (2009) Reduced structural connectivity in ventral visual cortex in congenital prosopagnosia. Nat Neurosci 12:29-31
9. Grüter T, Carbon CC (2010) Neuroscience. Escaping attention. Science 328(5977):435-436
10. Dobel C, Bolte J, Aicher M, Schweinberger SR (2007) Prosopagnosia without apparent cause: overview and diagnosis of six cases. Cortex 43:718-733 (Pubitemid 47189038)
11. Duchaine B, Nakayama K (2006) The Cambridge Face Memory Test: results for neurologically intact individuals and an investigation of its validity using inverted face stimuli and prosopagnosic participants. Neuropsychologia 44:576-585 (Pubitemid 43113381)
12. Duchaine BC, Parker H, Nakayama K (2003) Normal recognition of emotion in a prosopagnosic. Perception 32:827-838 (Pubitemid 37551011)
13. Duchaine BC, Dingle K, Butterworth E, Nakayama K (2004) Normal greeble learning in a severe case of developmental prosopagnosia. Neuron 43:469-473 (Pubitemid 39094674)
14. Dobel C, Putsche C, Zwitserlood P, Junghofer M (2008) Early left-hemispheric dysfunction of face processing in congenital prosopagnosia: an MEG study. PLoS ONE 3:e2326
15. Behrmann M, Avidan G, Gao F, Black S (2007) Structural imaging reveals anatomical alterations in inferotemporal cortex in congenital prosopagnosia. Cereb Cortex 17(10):2354-2363 (Pubitemid 47517471)
16. Garrido L, Furl N, Draganski B, Weiskopf N, Stevens J et al (2009) Voxel-based morphometry reveals reduced grey matter volume in the temporal cortex of developmental prosopagnosics. Brain 132:3443-3455
17. Avidan G, Hasson U, Malach R, Behrmann M (2005) Detailed exploration of face-related processing in congenital prosopagnosia: 2. Functional neuroimaging findings. J Cogn Neurosci 17:1150-1167 (Pubitemid 41045584)
18. Avidan G, Behrmann M (2009) Functional MRI reveals compromised neural integrity of the face processing network in congenital prosopagnosia. Curr Biol 19:1146-1150
19. Grueter M, Grueter T, Bell V, Horst J, Laskowski W et al (2007) Hereditary prosopagnosia: the first case series. Cortex 43:734-749 (Pubitemid 47189039)
20. Grüter T, Grüter M, Carbon CC (2008) Neural and genetic foundations of face recognition and prosopagnosia. J Neuropsychol 2(Pt 1):79-97
21. Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4:223-233 (Pubitemid 30332148)
22. Gobbini MI, Haxby JV (2007) Neural systems for recognition of familiar faces. Neuropsychologia 45:32-41 (Pubitemid 44821229)
23. Humphreys K, Minshew N, Leonard GL, Behrmann M (2007) A fine-grained analysis of facial expression processing in highfunctioning adults with autism. Neuropsychologia 45:685-695 (Pubitemid 44958746)
24. Grüter T, Grüter M (2007) Prosopagnosia in biographies and autobiographies. Perception 36:299-301
25. von Kriegstein K, Dogan O, Grüter M, Giraud AL, Kell CA et al (2008) Simulation of talking faces in the human brain improves auditory speech recognition. Proc Natl Acad Sci USA 105:6747-6752 (Pubitemid 351754578)
26. Grüter T, Grüter M, Carbon CC (2010) Congenital prosopagnosia: diagnosis and mental imagery: commentary on "Tree JJ, and Wilkie J. Face and object imagery in congenital prosopagnosia: a case series." Cortex
27. Ekman P, Friesen W (1976) Pictures of facial affects. Consulting Psychologist Press, Palo Alto
28. Cuthbert BN, Bradley MM, Lang PJ (1996) Probing picture perception: activation and emotion. Psychophysiology 33:103-111 (Pubitemid 26076320)
29. Lundqvist D, Litton JE (1998) The averaged Karolinska directed emotional faces-AKDEF: psychology section. Karolinska Institutet, Stockholm
30. Kesler-West ML, Andersen AH, Smith CD, Avison MJ, Davis CE et al (2001) Neural substrates of facial emotion processing using fMRI. Brain Res Cogn Brain Res 11:213-226 (Pubitemid 32245549)
31. Nakamura K, Kawashima R, Sato N, Nakamura A, Sugiura M et al (2000) Functional delineation of the human occipito-temporal areas related to face and scene processing. A PET study. Brain 123(Pt 9):1903-1912 (Pubitemid 30664293)
32. Lobmaier JS, Klaver P, Loenneker T, Martin E, Mast FW (2008) Featural and configural face processing strategies: evidence from a functional magnetic resonance imaging study. Neuroreport 19:287-291 (Pubitemid 351322964)
33. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ et al (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21-36 (Pubitemid 32552740)
34. Specht K, Minnerop M, Müller-Hübenthal J, Klockgether T (2005) Voxel-based analysis of multiple-system atrophy of cerebellar type: complementary results by combining voxel-based morphometry and voxel-based relaxometry. Neuroimage 25:287-293 (Pubitemid 40289156)
35. Friston KJ, Glaser DE, Henson RNA, Kiebel S, Phillips C et al (2002) Classical and Bayesian inference in neuroimaging: applications. Neuroimage 16:484-512 (Pubitemid 34852463)
36. Harmer CJ, Thilo KV, Rothwell JC, Goodwin GM (2001) Transcranial magnetic stimulation of medial-frontal cortex impairs the processing of angry facial expressions. Nat Neurosci 4:17-18 (Pubitemid 32095521)
37. Grüter T, Grüter M, Bell V, Carbon CC (2009) Visual mental imagery in congenital prosopagnosia. Neurosci Lett 453:135-140
38. Behrmann M, Avidan G, Marotta JJ, Kimchi R (2005) Detailed exploration of face-related processing in congenital prosopagnosia: 1. Behavioral findings. J Cogn Neurosci 17:1130-1149 (Pubitemid 41045583)
39. Yovel G, Duchaine B (2006) Specialized face perception mechanisms extract both part and spacing information: evidence from developmental prosopagnosia. J Cogn Neurosci 18:580-593 (Pubitemid 43763859)
40. Stollhoff R, Jost J, Elze T, Kennerknecht I (2010) The early time course of compensatory face processing in congenital prosopagnosia. PLoS One 5(7):e11482
41. Duchaine B, Germine L, Nakayama K (2007) Family resemblance: ten family members with prosopagnosia and within-class object agnosia. Cogn Neuropsychol 24:419-430 (Pubitemid 46917013)
42. Humphreys K, Minshew N, Leonard GL, Behrmann M (2007) A fine-grained analysis of facial expression processing in highfunctioning adults with autism. Neuropsychologia 45:685-695 (Pubitemid 44958746)
43. Aguirre GK, Zarahn E, D'Esposito M (1998) An area within human ventral cortex sensitive to "building" stimuli: evidence and implications. Neuron 21:373-383 (Pubitemid 28399697)
44. Levy I, Hasson U, Harel M, Malach R (2004) Functional analysis of the periphery effect in human building related areas. Hum Brain Mapp 22:15-26 (Pubitemid 38586097)
45. Levy I, Hasson U, Avidan G, Hendler T, Malach R (2001) Center-periphery organization of human object areas. Nat Neurosci 4:533-539 (Pubitemid 32397192)
46. Beauchamp MS, Lee KE, Haxby JV, Martin A (2003) FMRI responses to video and point-light displays of moving humans and manipulable objects. J Cogn Neurosci 15:991-1001 (Pubitemid 37281763)
47. Gorno-Tempini ML, Price CJ (2001) Identification of famous faces and buildings: a functional neuroimaging study of semantically unique items. Brain 124:2087-2097 (Pubitemid 32945906)
48. Mori S, Kaufmann WE, Davatzikos C, Stieltjes B, Amodei L et al (2002) Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn Reson Med 47:215-223 (Pubitemid 34116788)
49. Schmahmann JD, Pandya DN (2007) The complex history of the fronto-occipital fasciculus. J Hist Neurosci 16:362-377 (Pubitemid 350034875)
50. Rossion B, Caldara R, Seghier M, Schuller AM, Lazeyras F et al (2003) A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126:2381-2395 (Pubitemid 37314429)
51. Grill-Spector K, Kushnir T, Hendler T, Edelman S, Itzchak Y et al (1998) A sequence of object-processing stages revealed by fMRI in the human occipital lobe. Hum Brain Mapp 6:316-328 (Pubitemid 28364526)
52. Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302-4311 (Pubitemid 27220621)
53. Ishai A, Schmidt CF, Boesiger P (2005) Face perception is mediated by a distributed cortical network. Brain Res Bull 67:87-93 (Pubitemid 41225321)
54. Van den Stock J, van de Riet WA, Righart R, de Gelder B (2008) Neural correlates of perceiving emotional faces and bodies in developmental prosopagnosia: an event-related fMRI-study. PLoS One 3:e3195
55. Minnebusch DA, Suchan B, Koster O, Daum I (2009) A bilateral occipitotemporal network mediates face perception. Behav Brain Res 198:179-185
56. Ranganath C, Cohen MX, Dam C, D'Esposito M (2004) Inferior temporal, prefrontal, and hippocampal contributions to visual working memory maintenance and associative memory retrieval. J Neurosci 24:3917-3925 (Pubitemid 38544218)
57. Druzgal TJ, D'Esposito M (2001) A neural network reflecting decisions about human faces. Neuron 32:947-955 (Pubitemid 34024852)
58. Gazzaley A, Rissman J, D'Esposito M (2004) Functional connectivity during working memory maintenance. Cogn Affect Behav Neurosci 4:580-599 (Pubitemid 40342902)
59. Ranganath C, Cohen MX, Brozinsky CJ (2005) Working memory maintenance contributes to long-term memory formation: neural and behavioral evidence. J Cogn Neurosci 17:994-1010 (Pubitemid 41045573)
60. Kim H Dissociating the roles of the default-mode, dorsal, and ventral networks in episodic memory retrieval. Neuroimage 50:1648-1657
61. Blumenfeld RS, Parks CM, Yonelinas AP, Ranganath C (2011) Putting the pieces together: the role of dorsolateral prefrontal cortex in relational memory encoding. J Cogn Neurosci 23(1):257-265
62. Tree JJ, Wilkie J (2010) Face and object imagery in congenital prosopagnosia: a case series. Cortex 46(9):1189-1198
63. Bressler SL, Tang W, Sylvester CM, Shulman GL, Corbetta M (2008) Top-down control of human visual cortex by frontal and parietal cortex in anticipatory visual spatial attention. J Neurosci 28:10056-10061
64. Postle BR, Berger JS, Taich AM, D'Esposito M (2000) Activity in human frontal cortex associated with spatial working memory and saccadic behavior. J Cogn Neurosci 12(Suppl 2):2-14
65. Vuilleumier P, Pourtois G (2007) Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 45:174-194 (Pubitemid 44821236)
66. Harmer CJ, Thilo KV, Rothwell JC, Goodwin GM (2001) Transcranial magnetic stimulation of medial-frontal cortex impairs the processing of angry facial expressions. Nat Neurosci 4:17-18 (Pubitemid 32095521)
67. Keightley ML, Chiew KS, Anderson JA, Grady CL (2010) Neural correlates of recognition memory for emotional faces and scenes. Soc Cogn Affect Neurosci. doi:10.1093/scan/nsq003