Neural architecture underlying classification of face perception paradigms

NeuroImage

Volumn 119, Issue , 2015, Pages 70-80

  Laird, Angela R ^a   Riedel, Michael C ^a,b   Sutherland, Matthew T ^a   Eickhoff, Simon B ^c,d   Ray, Kimberly L ^b   Uecker, Angela M ^b   Fox, P Mickle ^b   Turner, Jessica A ^e   Fox, Peter T ^b,f,g  

^a FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e GEORGIA STATE UNIVERSITY   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

^g UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Cognitive paradigms; Face perception; Faces; Functional neuroimaging; Meta analysis; Neuroinformatics

Indexed keywords

ARTICLE; ATTENTION; CLASSIFICATION ALGORITHM; CONTROLLED STUDY; COORDINATION; CORRELATION ANALYSIS; DATA MINING; FACE; FEMALE; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MALE; NORMAL HUMAN; PERCEPTION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROBABILITY; RECOGNITION; SALIENCE NETWORK; VALIDATION PROCESS; VISUOSPATIAL ATTENTION; BRAIN; BRAIN MAPPING; CLUSTER ANALYSIS; EMOTION; FACIAL EXPRESSION; FACIAL RECOGNITION; IMAGE PROCESSING; METHODOLOGY; PHYSIOLOGY; PROCEDURES; RECALL;

ATTENTION; BRAIN; BRAIN MAPPING; CLUSTER ANALYSIS; DATA MINING; EMOTIONS; FACIAL EXPRESSION; FACIAL RECOGNITION; FUNCTIONAL NEUROIMAGING; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MENTAL RECALL; RECOGNITION (PSYCHOLOGY); RESEARCH DESIGN;

EID: 84936087673     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.06.044     Document Type: Article

References (98)

1. Belin P., Zatorre R.J., Lafaille P., Ahad P., Pike B. Voice-selective areas in human auditory cortex. Nature 2000, 403:309-312.
2. Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Working Group BRAIN 2025: a scientific vision. Report to the Advisory Committee to the Director 2014, NIH, (June 4, http://www.nih.gov/science/brain/2025/BRAIN2025.pdf).
3. 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.
4. Breiter H.C., Etcoff N.L., Whalen P.J., Kennedy W.A., Rauch S.L. Response and habituation of the human amygdala during visual processing of facial express. Neuron 1996, 17:875-887.
5. Brett M., Christoff K., Cusack R., Lancaster J. Using the Talairach atlas with the MNI template. Neuroimage 2001, 13:S85.
6. Bruce V., Young A. Understanding face recognition. Br. J. Psychol. 1986, 77:305-327.
7. Burton A.M., Bruce V., Johnston R.A. Understanding face recognition with an interactive activation model. Br. J. Psychol. 1990, 81:361-380.
8. Bzdok D., Langer R., Caspers S., Kurth F., Habel U., Zilles K., Laird A., Eickhoff S.B. ALE meta-analysis on facial judgements of trustworthiness and attractiveness. Brain Struct. Funct. 2011, 215:209-223.
9. Bzdok D., Langner R., Hoffstaedter F., Turetsky B.I., Zilles K., Eickhoff S.B. The modular neuroarchitecture of social judgements on faces. Cereb. Cortex 2012, 22:951-961.
10. Bzdok D., Langner R., Schilbach L., Jakobs O., Roski C., Caspers S., Laird A.R., Fox P.T., Zilles K., Eickhoff S.B. Characterization of the temporo-parietal junction by combining data-driven parcellation, complementary connectivity analyses, and functional decoding. Neuroimage 2013, 81:381-392.
11. Calvert G.A., Bullmore E.T., Brammer M.J., Campbell R., Williams S.C.R., McGuire P.K., Woodruff P.W.R., Iversen S.D., David A.S. Activation of auditory cortex during silent lipreading. Science 1997, 276:593-596.
12. Cauda F., D'Agata F., Sacco K., Duca S., Geminiani G., Vercelli A. Functional connectivity of the insula in the resting brain. Neuroimage 2011, 55:8-23.
13. Cauda F., Costa T., Torta D.M.E., Sacco K., D'Agata F., Duca S., Geminiani G., Fox P.T., Vercelli A. Meta-analytic clustering of the insular cortex: characterizing the meta-analytic connectivity of the insula when involved in active tasks. Neuroimage 2012, 62:343-355.
14. Chang L.J., Yarkoni T., Khaw M.W., Sanfey A.G. Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb. Cortex 2012, 23:739-749.
15. Cieslik E.C., Zilles K., Caspers S., Roski C., Kellerman T.S., Jakobs O., Langer R., Laird A.R., Fox P.T., Eickhoff S.B. Is there "one" DLPFC in cognitive action control? Evidence for heterogeneity from co-activation-based parcellation. Cereb. Cortex 2013, 23:2677-2698.
16. Clark V.P., Keil K., Maisog J.M., Courtney S., Ungerleider L.G., Haxby J.V. Functional magnetic resonance imaging of human visual cortex during face matching: a comparison with positron emission tomography. Neuroimage 1996, 4:1-15.
17. Clos M., Amunts K., Laird A.R., Fox P.T., Eickhoff S.B. Tackling the multifunctional nature of Broca's region meta-analytically: co-activation-based parcellation of area 44. Neuroimage 2013, 83:174-188.
18. Collins D.L., Neelin P., Peters T.M., Evans A.C. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 1994, 18:192-205.
19. Craig A.D. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 2002, 3:655-666.
20. Craig A.D. How do you feel - now? The anterior insula and human awareness. Nat. Rev. Neurosci. 2009, 10:59-70.
21. Damasio H., Grabowski T.J., Tranel D., Hichwa R.D., Damasio A.R. A neural basis for lexical retrieval. Nature 1996, 380:499-505.
22. De Martino B., Kalisch R., Rees G., Dolan R.J. Enhanced processing of threat stimuli under limited attentional resources. Cereb. Cortex 2009, 19:127-133.
23. Deen B., Pitskel N.B., Pelphrey K.A. Three systems of insular functional connectivity identified with cluster analysis. Cereb. Cortex 2011, 21:1498-1506.
24. Druzgal T.J., D'Esposito M. A neural network reflecting decisions about human faces. Neuron 2001, 32:947-955.
25. Eickhoff S.B., Laird A.R., Grefkes C., Wang L.E., Zilles K., Fox P.T. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum. Brain Mapp. 2009, 30:2907-2926.
26. Eickhoff S.B., Bzdok D., Laird A.R., Kurth F., Fox P.T. Activation likelihood estimation revisited. Neuroimage 2012, 59:2349-2361.
27. Evans A.C., Collins D.L., Mills S.R., Brown E.D., Kelly R.L., Peters T.M. 3D statistical neuroanatomical models from 305 MRI volumes. Proceedings of IEEE-Nuclear Science Symposium and Medical Imaging Conference 1993, 1813-1817.
28. Fox P.T., Lancaster J.L. Mapping context and content: the BrainMap model. Nat. Rev. Neurosci. 2002, 3:319-321.
29. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9673-9678.
30. Fusar-Poli P., Placentino A., Carletti F., Landi P., Allen P., Surguladze S., Benedetti F., Abbamonte M., Gasparotti R., Barale F., Perez J., McGuire P., Politi P. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J. Psychiatry Neurosci. 2009, 34:418-432.
31. Gobbini M.I., Haxby J.V. Neural systems for recognition of familiar faces. Neuropsychologia 2007, 45:32-41.
32. Gorno Tempini M.L., Price C.J., Josephs O., Vandenberghe R., Cappa S.F., Kapur N., Frackowiak R.S.J. The neural systems sustaining face and proper-name processing. Brain 1998, 121:2103-2118.
33. Grosbras M.H., Laird A.R., Paus T. Cortical regions involved in eye movements, shifts of attention, and gaze perception. Hum. Brain Mapp. 2005, 25:140-154.
34. Halgren E., Dale A.M., Sereno M.I., Tootell R.B.H., Marinkovic K., Rosen B.R. Location of human face-selective cortex with respect to retinotopic areas. Hum. Brain Mapp. 1999, 7:29-37.
35. Hariri A.R., Bookheimer S.Y., Mazziotta J.C. Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport 2000, 11:43-48.
36. Haxby J.V., Horwitz B., Ungerleider L.G., Maisog J.M., Pietrini P., Grady C.L. The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations. J. Neurosci. 1994, 14:6336-6353.
37. Haxby J.V., Ungerleider L.G., Clark V.P., Schouten J.L., Hoffman E.A., Martin A. The effect of face inversion on activity in human neural systems for face and object perception. Neuron 1999, 22:189-199.
38. Haxby J.V., Hoffman E.A., Gobbini M.I. Human neural systems for face recognition and social communication. Biol. Psychiatry 2002, 51:59-67.
39. Heekeren H.R., Marrett S., Ruff D.A., Bandettini P.A., Ungerleider L.G. Involvement of human left dorsolateral prefrontal cortex in perceptual decision making is independent of response modality. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10023-10028.
40. Ho S.S., Gonzalez R.D., Abelson J.L., Liberzon I. Neurocircuits underlying cognition-emotion interaction in a social decision making context. Neuroimage 2012, 63:843-857.
41. Hoffman E.A., Haxby J.V. Distinct representations of eye gaze and neural identify in the distributed human neural system for face perception. Nat. Neurosci. 2000, 3:80-84.
42. Insel T., Cuthbert B., Garvey M., Heinssen R., Pine D.S., Quinn K., Sanislow C., Wang P. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am. J. Psychiatry 2010, 167:748-751.
43. Ishai A., Ungerleider L.G., Martin A., Schouten J.L., Haxby J.V. Distributed representation of objects in the human ventral visual pathway. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9379-9384.
44. Ishai A., Schmidt C.F., Boesiger P. Face perception is mediated by a distributed cortical network. Brain Res. Bull. 2005, 67:87-93.
45. Kampe K.K., Frith C.D., Dolan R.J., Frith U. Reward value of attractiveness and gaze. Nature 2001, 413:589.
46. Kanwisher N., McDermott J., Chun M.M. The fusiform face area: a model in human extrastriate cortex specialized for face perception. J. Neurosci. 1997, 17:4302-4311.
47. Keilholz S.D., Magnuson M., Thompson G. Evaluation of data-driven network analysis approaches for functional connectivity MRI. Brain Struct. Funct. 2010, 215:129-140.
48. Kelly C., Uddin L.Q., Shehzad Z., Margulies D.S., Castellanos F.X., Milham M.P., Petrides M. Broca's region: linking human brain functional connectivity data and non-human primate tracing anatomy studies. Eur. J. Neurosci. 2010, 32:383-398.
49. Krall S.C., Rottschy C., Oberwelland E., Bzdok D., Fox P.T., Eickhoff S.B., Fink G.R., Konrad K. The role of the right temporoparietal junction in attention and social interaction as revealed by ALE meta-analysis. Brain Struct. Funct. 2015, 220(2):587-604.
50. Kurth F., Zilles K., Fox P.T., Laird A.R., Eickhoff S.B. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 2010, 214:519-534.
51. Laird A.R., Lancaster J.L., Fox P.T. BrainMap: the social evolution of a functional neuroimaging database. Neuroinformatics 2005, 3:65-78.
52. Laird A.R., Fox M., Price C.J., Glahn D.C., Uecker A.M., Lancaster J.L., Turkeltaub P.E., Kochunov P., Fox P.T. ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum. Brain Mapp. 2005, 25:155-164.
53. Laird A.R., Eickhoff S.B., Li K., Robin D.A., Glahn D.C., Fox P.T. Investigating the functional heterogeneity of the default mode network using coordinate-based meta-analytic modeling. J. Neurosci. 2009, 29:14496-14505.
54. Laird A.R., Robinson J.L., McMillan K.M., Tordesillas-Gutierrez D., Moran S.T., Ray K.L., Franklin C., Glahn D.C., Fox P.T., Lancaster J.L. Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: validation of the Lancaster transform. Neuroimage 2010, 51:677-683.
55. Laird A.R., Eickhoff S.B., Fox P.M., Uecker A.M., Ray K.L., Saenz J.J., McKay D.R., Bzdok D., Laird R.W., Robinson J.L., Turner J.A., Turkeltaub P.E., Lancaster J.L., Fox P.T. The BrainMap strategy for standardization, sharing, and meta-analysis of neuroimaging data. BMC Res. Notes 2011, 4:349.
56. Laird A.R., Fox P.M., Eickhoff S.B., Turner J.A., Ray K.L., McKay D.R., Glahn D.C., Beckmann C.F., Smith S.M., Fox P.T. Behavioral interpretations of intrinsic connectivity networks. J. Cogn. Neurosci. 2011, 23:4022-4037.
57. Lancaster J.L., Tordesillas-Gutiérrez D., Martinez M., Salinas F., Evans A., Zilles K., Mazziotta J.C., Fox P.T. Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum. Brain Mapp. 2007, 28:1194-1205.
58. 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. J. Neurosci. 2000, 20:878-886.
59. Liu X., Zhu X.H., Qiu P., Chen W. A correlation-matrix-based hierarchical clustering method for functional connectivity analysis. J. Neurosci. Methods 2012, 211:94-102.
60. Luo Y., Qin S., Fernandez G., Zhang Y., Klumpers F., Li H. Emotion perception and executive control interact in the salience network during emotionally charged working memory. Hum. Brain Mapp. 2014, 35:5606-5616.
61. Markram H. The human brain project. Sci. Am. 2012, 306:50-55.
62. Martinelli P., Sperduti M., Piolino P. Neural substrates of the self-memory system: new insights from a meta-analysis. Hum. Brain Mapp. 2013, 34:1515-1529.
63. McCarthy G., Puce A., Gore J.C., Allison T. Face-specific processing in the human fusiform gyrus. J. Cogn. Neurosci. 1997, 9:605-610.
64. Menon V., Uddin L.Q. Saliency, switching, attention, and control: a network model of insula function. Brain Struct. Funct. 2010, 214:655-667.
65. Morris J.S., Frith C.D., Perrett D.I., Rowland D., Young A.W., Calder A.J., Dolan R.J. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 1996, 383:812-815.
66. Nahum L., Simon S.R., Sander D., Lazeyras F., Schnider A. Neural response to the behaviorally relevant absence of anticipated outcomes and the presentation of potentially harmful stimuli: a human fMRI study. Cortex 2011, 47:191-201.
67. Nickl-Jockschat T., Rottschy C., Thommes J., Schneider F., Laird A.R., Fox P.T., Eickhoff S.B. Neural networks related to dysfunctional face processing in autism spectrum disorder. Brain Struct. Funct. 2015, (In Press).
68. Paulesu E., Perani D., Biasi V., Silani G., Borghese N.A., De Giovanni U., Sensolo S., Fazio F. A functional-anatomical model for lipreading. J. Neurophysiol. 2003, 90:2005-2013.
69. Pedrycz W. Knowledge-Based Clustering: From Data to Information Granules 2005, John Wiley, Hoboken, NJ.
70. Phillips M.L., Young A.W., Scott S.K., Calder A.J., Andrew C., Giampietro V., Williams S.C.R., Bullmore E.T., Brammer M., Gray J.A. Neural responses to facial and vocal expressions of fear and disgust. Proc. R. Soc. Lond. B 1998, 265:1809-1817.
71. Poldrack R.A. Can cognitive processes be inferred from neuroimaging data?. Trends Cogn. Sci. 2006, 10:59-63.
72. Poldrack R.A., Kittur A., Kalar D., Miller E., Seppa C., Gil Y., Parker D.S., Sabb F.W., Bilder R.M. The cognitive atlas: toward a knowledge foundation for cognitive neuroscience. Front Neuroinform 2011, 5:17.
73. Price C.J., Devlin J.T., Moore C.J., Morton C., Laird A.R. Meta-analyses of object naming: effect of baseline. Hum. Brain Mapp. 2005, 25:70-82.
74. Puce A., Allison T., Bentin S., Gore J.C., McCarthy G. Temporal cortex activation in humans viewing eye and mouth movements. J. Neurosci. 1998, 18:2188-2199.
75. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:676-682.
76. Ramasubbu R., Masalovich S., Peltier S., Holtzheimer P.I., Heim C., Mayberg H.S. Neural representation of maternal face processing: a functional magnetic resonance imaging study. Can. J. Psychiatry 2007, 52:726-734.
77. Ramasubbu R., Masalovich S., Gaxiola I., Peltier S., Hotzheimer P.E., Heim C., Goodyear B., MacQueen G., Mayberg H.S. Differential neural activity and connectivity for processing one's own face: a preliminary report. Psych. Res. 2011, 194:130-140.
78. Rolls E.T. The representation of information about faces in the temporal and frontal lobes. Neuropsychologia 2007, 45:124-143.
79. 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. Hum. Brain Mapp. 2009, 30:2821-2833.
80. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
81. Sergent J., Ohta S., MacDonald B. Functional neuroanatomy of face and object processing: a positron emission tomography study. Brain 1992, 115:15-36.
82. Shah N.J., Marshall J.C., Zafiris O., Schwab A., Zilles K., Markowitsch H.J., Fink G.R. The neural correlates of person familiarity: a functional magnetic resonance imaging study with clinical implications. Brain 2001, 124:804-815.
83. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
84. Shi H., Wang X., Yao S. Comparison of activation patterns between masking and inattention tasks: a coordinate-based meta-analysis of implicit emotional face processing. Front. Hum. Neurosci. 2013, 7:459.
85. Simon D., Becker M.P.I., Mothes-Lasch M., Miltner W.H.R., Straube T. Effects of social context on feedback-related activity in the human ventral striatum. Neuroimage 2014, 99:1-6.
86. Spreng R.N., Mar R.A., Kim A.S.N. The common neural basis of autobiographical memory, prospection, navigation, theory of mind, and the default mode: a quantitative meta-analysis. J. Cogn. Neurosci. 2009, 21:489-510.
87. Sreenivas S., Boehm S.G., Linden D.E.J. Emotional faces and the default mode network. Neurosci. Lett. 2012, 506:229-234.
88. Talairach J., Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain 1988, Thieme Medical Publishers, New York.
89. Taylor K.S., Seminowicz D.A., Davis K.D. Two systems of resting state connectivity between the insula and cingulate cortex. Hum. Brain Mapp. 2009, 30:2731-2745.
90. Toga A.W., Clark K.A., Thompson P.M., Shattuck D.W., Van Horn J.D. Mapping the human connectome. Neurosurgery 2012, 71:1-5.
91. Turkeltaub P.E., Eden G.F., Jones K.M., Zeffiro T.A. Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 2002, 16:765-780.
92. Turkeltaub P.E., Eickhoff S.B., Laird A.R., Fox P.M., Wiener M., Fox P.T. Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum. Brain Mapp. 2012, 33:1-13.
93. Turner J.A., Laird A.R. The cognitive paradigm ontology: design and application. Neuroinformatics 2012, 10:57-66.
94. Turner M.D., Chakrabarti C., Jones T.B., Xu J.F., Fox P.T., Luger G.F., Laird A.R., Turner J.A. Automated annotation of functional neuroimaging experiments via multi-label classification. Front. Neurosci. Brain Imag Methods 2013, 7:240.
95. Van Essen D.C., Smith S.M., Barch D.M., Behrens T.E.J., Yacoub E. Ugurbil K, for the WU-Minn HCP consortium. The WU-Minn human connectome project: an overview. NeuroImage 2013, 80:62-79.
96. Woo C.W., Krishnan A., Wager T.D. Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. Neuroimage 2014, 91:412-4129.
97. Yarkoni T., Poldrack R.A., Nichols T.E., Van Essen D.C., Wager T.D. Large-scale automated synthesis of human functional neuroimaging data. Nat. Methods 2011, 8:665-670.
98. Zhen Z., Fang H., Liu J. The hierarchical brain network for face recognition. PLoS ONE 2013, 8:e59886.