Covert face recognition without the fusiform-temporal pathways

NeuroImage

Volumn 57, Issue 3, 2011, Pages 1162-1176

  Valdés Sosa, Mitchell ^a   Bobes, Maria A ^a   Quiñones, Ileana ^a   Garcia, Lorna ^a   Valdes Hernandez, Pedro A ^a   Iturria, Yasser ^a   Melie Garcia, Lester ^a   Lopera, Francisco ^b   Asencio, José ^c  

^a CENTRO DE NEUROCIENCIAS DE CUBA   (Cuba)

^b UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^c Epilepsy Section   (Colombia)

Author keywords

Faces; Functional imaging; Prosopagnosia; Tractography

Indexed keywords

ADULT; AGED; ARTICLE; CASE REPORT; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FACE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM FACE AREA; FUSIFORM GYRUS; HUMAN; INFERIOR LONGITUDINAL BUNDLE; MALE; NERVE CELL MEMBRANE POTENTIAL; NERVE TRACT; OCCIPITAL GYRUS; ORBITAL CORTEX; POSTERIOR CINGULATE; PRIORITY JOURNAL; PROSOPAGNOSIA; RECOGNITION; RIGHT HEMISPHERE; TEMPORAL LOBE; TEMPORAL SUMMATION;

AGED; BRAIN; BRAIN MAPPING; DIFFUSION TENSOR IMAGING; FACE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PATTERN RECOGNITION, VISUAL; PROSOPAGNOSIA;

EID: 79959711158     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.04.057     Document Type: Article

References (89)

1. Ashburner J., Friston K.J. Unified segmentation. Neuroimage 2005, 26:839-851.
2. Avidan G., Behrmann M. Functional MRI reveals compromised neural integrity of the face processing network in congenital prosopagnosia. Curr. Biol. 2009, 19:1146-1150.
3. Barbeau E.J., Taylor M.J., Regis J., Marquis P., Chauvel P., Liegeois-Chauvel C. Spatio temporal dynamics of face recognition. Cereb. Cortex 2008, 18:997-1009.
4. Barton J.J., Cherkasova M.V., Hefter R. The covert priming effect of faces in prosopagnosia. Neurology 2004, 63:2062-2068.
5. Barton J.J., Press D.Z., Keenan J.P., O'Connor M. Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia. Neurology 2002, 58:71-78.
6. Barton J.J.S., Cherkasova M., O'Connor M. Covert recognition in acquired and developmental prosopagnosia. Neurology 2001, 57:1161-1168.
7. Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 1996, 111(3):209-219.
8. Bate S., Haslam C., Jansari A., Hodgson T.L. Covert face recognition relies on affective valence in congenital prosopagnosia. Cogn. Neuropsychol. 2009, 1-21.
9. Bauer R.M. Autonomic recognition of names and faces in prosopagnosia: a neuropsychological application of the Guilty Knowledge Test. Neuropsychologia 1984, 22:457-469.
10. Behrmann M., Avidan G. Congenital prosopagnosia: face-blind from birth. Trends Cogn. Sci. 2005, 9:180-187.
11. Bobes M.A., Lopera F., Díaz Comas L., Galan L., Carbonell F., Bringas M.L., Valdés-Sosa M. Brain potentials reflect residual face processing in a case of prosopagnosia. Cogn. Neuropsychol. 2004, 21:691-718.
12. Bodamer A. Die prosopagnosia. Arch. Psychiatr. Nervenkr. 1947, 179:6-53.
13. Bouvier S.E., Engel S.A. Behavioral deficits and cortical damage loci in cerebral achromatopsia. Cereb. Cortex 2006, 16:183-191.
14. Breen N., Caine D., Coltheart M. Models of face recognition and delusional misidentification: a critical review. Cogn. Neuropsychol. 2000, 17:55-71.
15. Brett M., Leff A.P., Rorden C., Ashburner J. Spatial normalization of brain images with focal lesions using cost function masking. Neuroimage 2001, 14:486-500.
16. Bruyer R., Laterre C., Seron X., Feyereisen P., Strypstein E., Pierrard E., Rectem D. A case of prosopagnosia with some preserved covert remembrance of familiar faces. Brain Cogn. 1983, 2:257-284.
17. Bukach C.M., Bub D.N., Gauthier I., Tarr M.J. Perceptual expertise effects are not all or none: spatially limited perceptual expertise for faces in a case of prosopagnosia. J. Cogn. Neurosci. 2006, 18:48-63.
18. Bullmore E.T., Suckling J., Overmeyer S., Rabe-Hesketh S., Taylor E., Brammer M.J. Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans. Med. Imaging 1999, 18:32-42.
19. Catani M., Jones D.K., Donato R., Ffytche D.H. Occipito-temporal connections in the human brain. Brain 2003, 126:2093-2107.
20. Caramazza A. The logic of neuropsychological research and the problem of patient classification in aphasia. Brain Lang. 1984, 21:9-20.
21. Caramazza A., McCloskey M. The case for single-patient studies. Cogn. Neuropsychol. 1988, 5:517-527.
22. Chatterjee A., Thomas A., Smith S.E., Aguirre G.K. The neural response to facial attractiveness. Neuropsychology 2009, 23:135-143.
23. Cohen Kadosh K., Walsh V., Cohen Kadosh R. Investigating face-property specific processing in the right OFA. Soc. Cogn. Affect. Neurosci. 2011, 6:58-65.
24. Collignon A., Maes F., Delaere D., Vandermeulen D., Suetens P., Marchal G. Automated multi-modality image registration based on information theory. Information Processing in Medical Imaging 1995, 263-274. Kluwer Academic Publishers, Dordrecht. Y. Bizais, C. Barillot, R. Di Paola (Eds.).
25. Crawford J.R., Garthwaite P.H. Investigation of the single case in neuropsychology: confidence limits on the abnormality of test scores and test score differences. Neuropsychologia 2002, 40:1196-1208.
26. Critchley H.D., Elliott R., Mathias C.J., Dolan R.J. Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study. J. Neurosci. 2000, 20:3033-3040.
27. De Haan E.H., Bauer R.M., Greve K.W. Behavioural and physiological evidence for covert face recognition in a prosopagnosic patient. Cortex 1992, 28:77-95.
28. Diedrichsen J., Shadmehr R. Detecting and adjusting for artifacts in fMRI time series data. Neuroimage 2005, 27:624-634.
29. Dricot L., Sorger B., Schiltz C., Goebel R., Rossion B. The roles of "face" and "non-face" areas during individual face perception: evidence by fMRI adaptation in a brain-damaged prosopagnosic patient. Neuroimage 2008, 40:318-332.
30. Dubois S., Rossion B., Schiltz C., Bodart J.M., Michel C., Bruyer R., Crommelinck M. Effect of familiarity on the processing of human faces. Neuroimage 1999, 9:278-289.
31. Fairhall S.L., Ishai A. Effective connectivity within the distributed cortical network for face perception. Cereb. Cortex 2007, 17:2400-2406.
32. Farah M.J., O'Reilly R.C., Vecera S.P. Dissociated overt and covert recognition as an emergent property of a lesioned neural network. Psychol. Rev. 1993, 100:571-588.
33. Fox C.J., Iaria G., Barton J.J. Disconnection in prosopagnosia and face processing. Cortex 2008, 44:996-1009.
34. Gainotti G. Different patterns of famous people recognition disorders in patients with right and left anterior temporal lesions: a systematic review. Neuropsychologia 2007, 45:1591-1607.
35. Garthwaite P.H., Crawford J.R. The distribution of the difference between two t-variates. Biometrika 2004, 91:987-994.
36. George N., Dolan R.J., Fink G.R., Baylis G.C., Russell C., Driver J. Contrast polarity and face recognition in the human fusiform gyrus. Nat. Neurosci. 1999, 2:574-580.
37. Gilaie-Dotan S., Malach R. Sub-exemplar shape tuning in human face-related areas. Cereb. Cortex 2007, 17:325-338.
38. Gilboa A., Alain C., He Y., Stuss D.T., Moscovitch M. Ventromedial prefrontal cortex lesions produce early functional alterations during remote memory retrieval. J. Neurosci. 2009, 29:4871-4881.
39. Gobbini M.I., Haxby J.V. Neural systems for recognition of familiar faces. Neuropsychologia 2007, 45:32-41.
40. Gobbini M.I., Leibenluft E., Santiago N., Haxby J.V. Social and emotional attachment in the neural representation of faces. Neuroimage 2004, 22:1628-1635.
41. Hadjikhani N., de Gelder B. Neural basis of prosopagnosia: an fMRI study. Hum. Brain Mapp. 2002, 16:176-182.
42. Haxby J.V., Hoffman E.A., Gobbini M.I. The distributed human neural system for face perception. Trends Cogn. Sci. 2000, 4:223-233.
43. Heller R., Golland Y., Malach R., Benjamini Y. Conjunction group analysis: an alternative to mixed/random effect analysis. Neuroimage 2007, 37:1178-1185.
44. Hua K., Oishi K., Zhang J., Wakana S., Yoshioka T., Zhang W., Akhter K.D., Li X., Huang H., Jiang H., van Z.P., Mori S. Mapping of functional areas in the human cortex based on connectivity through association fibers. Cereb. Cortex 2009, 19:1889-1895.
45. Hubbard P.L., Parker G. Validation of tractography. Diffusion MRI: From Quantitative Measurement to In-vivo Neuroanatomy, First Edition Ed 2009, 353-376. Academic Press, London. H. Johansen-Berg, T.E. Behrens (Eds.).
46. Huizenga H.M., Smeding H., Grasman R.P., Schmand B. Multivariate normative comparisons. Neuropsychologia 2007, 45:2534-2542.
47. Johansen-Berg H., Behrens T.E., Robson M.D., Drobnjak I., Rushworth M.F., Brady J.M., Smith S.M., Higham D.J., Matthews P.M. Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13335-13340.
48. Josephs K.A., Whitwell J.L., Vemuri P., Senjem M.L., Boeve B.F., Knopman D.S., Smith G.E., Ivnik R.J., Petersen R.C., Jack C.R. The anatomic correlate of prosopagnosia in semantic dementia. Neurology 2008, 71:1628-1633.
49. Kim D.S., Kim M. Combining functional and diffusion tensor MRI. Ann. N.Y. Acad. Sci. 2005, 1064:1-15.
50. Kreher B.W., Schnell S., Mader I., Il'yasov K.A., Hennig J., Kiselev V.G., Saur D. Connecting and merging fibres: pathway extraction by combining probability maps. Neuroimage 2008, 43:81-89.
51. Kringelbach M.L., Rolls E.T. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog. Neurobiol. 2004, 72:341-372.
52. Lanyon L.J., Scheel M., Fox C.J., Iaria G., Barton J.J.S. Disconnection of cortical face network in prosopagnosia revealed by diffusion tensor imaging. J. Vis. 2009, 9:482.
53. Lawes I.N., Barrick T.R., Murugam V., Spierings N., Evans D.R., Song M., Clark C.A. Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage 2008, 39:62-79.
54. Lopera F., Ardila A. Prosopamnesia and visuolimbic disconnection syndrome: a case study. Neuropsychology 1992, 6:3-12.
55. Marotta J.J., Genovese C.R., Behrmann M. A functional MRI study of face recognition in patients with prosopagnosia. Neuroreport 2001, 12:1581-1587.
56. Meadows J.C. The anatomical basis of prosopagnosia. J. Neurol. Neurosurg. Psychiatry 1974, 37:489-501.
57. Mori S., Crain B.J., Chacko V.P., van Zijl P.C. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 1999, 45:265-269.
58. Mori S., Oishi K., Jiang H., Jiang L., Li X., Akhter K., Hua K., Faria A.V., Mahmood A., Woods R., Toga A.W., Pike G.B., Neto P.R., Evans A., Zhang J., Huang H., Miller M.I., van Z.P., Mazziotta J. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 2008, 40:570-582.
59. Moore D.S., McCabe G.P. Introduction to the Practice of Statistics 2006, W.H. Freeman and Company, New York. 5th ed.
60. Nagai C. Neural mechanisms of facial recognition. Brain Nerve 2007, 59:45-51.
61. Parker G.J., Haroon H.A., Wheeler-Kingshott C.A. A framework for a streamline-based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements. J. Magn. Reson. Imaging 2003, 18:242-254.
62. Philippi C.L., Mehta S., Grabowski T., Adolphs R., Rudrauf D. Damage to association fiber tracts impairs recognition of the facial expression of emotion. J. Neurosci. 2009, 29:15089-15099.
63. Raz J., Zheng H., Ombao H., Turetsky B. Statistical tests for fMRI based on experimental randomization. Neuroimage 2003, 19:226-232.
64. Renault B., Signoret J., Debruille B., Breton F., Bolgert F. Brain potentials reveal covert facial recognition in prosopagnosia. Neuropsychologia 1989, 27:905-912.
65. Rossion B. Constraining the cortical face network by neuroimaging studies of acquired prosopagnosia. Neuroimage 2008, 40:423-426.
66. Rudrauf D., David O., Lachaux J.P., Kovach C.K., Martinerie J., Renault B., Damasio A. Rapid interactions between the ventral visual stream and emotion-related structures rely on a two-pathway architecture. J. Neurosci. 2008, 28:2793-2803.
67. Saur D., Schelter B., Schnell S., Kratochvil D., Kupper H., Kellmeyer P., Kummerer D., Kloppel S., Glauche V., Lange R., Mader W., Feess D., Timmer J., Weiller C. Combining functional and anatomical connectivity reveals brain networks for auditory language comprehension. Neuroimage 2010, 49:3187-3197.
68. Schiltz C., Sorger B., Caldara R., Ahmed F., Mayer E., Goebel R., Rossion B. Impaired face discrimination in acquired prosopagnosia is associated with abnormal response to individual faces in the right middle fusiform gyrus. Cereb. Cortex 2006, 16:574-586.
69. Schwartzman A., Dougherty R.F., Lee J., Ghahremani D., Taylor J.E. Empirical null and false discovery rate analysis in neuroimaging. Neuroimage 2009, 44:71-82.
70. Schweinberger S.R., Burton A.M. Covert recognition and the neural system for face processing. Cortex 2003, 39:9-30.
71. Sergent J., Signoret J.L. Implicit access to knowledge derived from unrecognized faces in prosopagnosia. Cereb. Cortex 1992, 2:389-400.
72. Sergent J., Signoret J.L. Varieties of functional deficits in prosopagnosia. Cereb. Cortex 1992, 2:375-388.
73. Shallice T. From Neuropsychology to Mental Structure 1988, Cambridge University Press, Cambridge England and New York.
74. Shattuck D.W., Mirza M., Adisetiyo V., Hojatkashani C., Salamon G., Narr K.L., Poldrack R.A., Bilder R.M., Toga A.W. Construction of a 3D probabilistic atlas of human cortical structures. Neuroimage 2008, 39:1064-1080.
75. Simon S.R., Khateb A., Darque A., Lazeyras F., Mayer E., Pegna A.J. When the brain remembers, but the patient doesn't: converging fMRI and EEG evidence for covert recognition in a case of prosopagnosia. Cortex 2010, 10.1016/j.cortex.2010.07.009.
76. Sorger B., Goebel R., Schiltz C., Rossion B. Understanding the functional neuroanatomy of acquired prosopagnosia. Neuroimage 2007, 35:836-852.
77. Steeves J., Dricot L., Goltz H.C., Sorger B., Peters J., Milner A.D., Goodale M.A., Goebel R., Rossion B. Abnormal face identity coding in the middle fusiform gyrus of two brain-damaged prosopagnosic patients. Neuropsychologia 2009, 47:2584-2592.
78. Steeves J.K., Culham J.C., Duchaine B.C., Pratesi C.C., Valyear K.F., Schindler I., Humphrey G.K., Milner A.D., Goodale M.A. The fusiform face area is not sufficient for face recognition: evidence from a patient with dense prosopagnosia and no occipital face area. Neuropsychologia 2006, 44:594-609.
79. Thomas C., Avidan G., Humphreys K., Jung K.J., Gao F., Behrmann M. Reduced structural connectivity in ventral visual cortex in congenital prosopagnosia. Nat. Neurosci. 2009, 12:29-31.
80. Thomas C., Avidan G., Jung K.-J., Behrmann M. Disruption in structural connectivity in ventral cortex in congenital prosopagnosia. J. Vis. 2006, 6:88.
81. Tranel D., Damasio A.R. The covert learning of affective valence does not require structures in hippocampal system or amygdala. J. Cogn. Neurosci. 1993, 5:79-88.
82. Tranel D., Damasio A.R. Knowledge without awareness: an autonomic index of facial recognition by prosopagnosics. Science 1985, 228:1453-1454.
83. Tranel D., Damasio H., Damasio A.R. Double dissociation between overt and covert face recognition. J. Cogn. Neurosci. 1995, 7:425-432.
84. Tuch D.S. Q-ball imaging. Magn. Reson. Med. 2004, 52:1358-1372.
85. Van den Stock J., van de Riet W.A., Righart R., de Gelder B. Neural correlates of perceiving emotional faces and bodies in developmental prosopagnosia: an event-related fMRI-study. PLoS One 2008, 3.9:e3195.
86. Wedeen V.J., Hagmann P., Tseng W.Y., Reese T.G., Weisskoff R.M. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn. Reson. Med. 2005, 54:1377-1386.
87. Yamasaki T., Taniwaki T., Tobimatsu S., Arakawa K., Kuba H., Maeda Y., Kuwabara Y., Shida K., Ohyagi Y., Yamada T., Kira J. Electrophysiological correlates of associative visual agnosia lesioned in the ventral pathway. J. Neurol. Sci. 2004, 221(1-2):53-60.
88. Young A.W. Conscious and nonconscious recognition of familiar faces. Attention and Performance XV Conscious and Nonconscious Information Processing 1994, 153-178. MIT Press/Bradford Books, Cambridge, MA. C. Umiltá, M. Moscovitch (Eds.).
89. Young A.W., Burton A.M. Simulating face recognition: implication for modelling cognition. Cogn. Neuropsychol. 1999, 16:1-48.