FMRI evidence of neural abnormalities in the subcortical face processing system in ASD

NeuroImage

Volumn 54, Issue 1, 2011, Pages 697-704

  Kleinhans, Natalia M ^a,b   Richards, Todd ^a,b   Johnson, L Clark ^b   Weaver, Kurt E ^a   Greenson, Jessica ^b   Dawson, Geraldine ^b   Aylward, Elizabeth ^b,c  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Seattle Children's Research Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; AUTISM; BEHAVIOR; BRAIN FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; FACE; FEAR; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; INTELLIGENCE QUOTIENT; NEUROIMAGING; ORIENTATION; PERCEPTION; PRIORITY JOURNAL;

ADOLESCENT; ADULT; AMYGDALA; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; EMOTIONS; FACE; FACIAL EXPRESSION; FEAR; GYRUS CINGULI; HUMANS; INTELLIGENCE; MAGNETIC RESONANCE IMAGING; MASKS; PATTERN RECOGNITION, VISUAL;

EID: 77957946858     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.07.037     Document Type: Article

References (94)

1. Adolphs R., Tranel D. Amygdala damage impairs emotion recognition from scenes only when they contain facial expressions. Neuropsychologia 2003, 41:1281-1289.
2. Adolphs R., Sears L., Piven J. Abnormal processing of social information from faces in autism. J. Cogn. Neurosci. 2001, 13:232-240.
3. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 1994, American Psychiatric Association, Washington, DC. 4th ed.
4. Ashwin C., Chapman E., Colle L., Baron-Cohen S. Impaired recognition of negative basic emotions in autism: a test of the amygdala theory. Soc. Neurosci. 2006, 1:349-363.
5. Ashwin C., Baron-Cohen S., Wheelwright S., O'Riordan M., Bullmore E.T. Differential activation of the amygdala and the 'social brain' during fearful face-processing in Asperger syndrome. Neuropsychologia 2007, 45(1):2-14.
6. Aylward E.H., Minshew N.J., Goldstein G., Honeycutt N.A., Augustine A.M., Yates K.O., Barta P.E., Pearlson G.D. MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology 1999, 53:2145-2150.
7. Aylward E.H., Park J.E., Field K.M., Parsons A.C., Richards T.L., Cramer S.C., Meltzoff A.N. Brain activation during face perception: evidence of a developmental change. J. Cogn. Neurosci. 2005, 17:308-319.
8. Bird G., Catmur C., Silani G., Frith C., Frith U. Attention does not modulate neural responses to social stimuli in autism spectrum disorders. Neuroimage 2006, 31:1614-1624.
9. Boucher J., Lewis V., Collis G. Familiar face and voice matching and recognition in children with autism. J. Child Psychol. Psychiatry 1998, 39:171-181.
10. Braeutigam S., Bailey A.J., Swithenby S.J. Task-dependent early latency (30-60ms) visual processing of human faces and other objects. NeuroReport 2001, 12:1531-1536.
11. Bryant R.A., Kemp A.H., Felmingham K.L., Liddell B., Olivieri G., Peduto A., Gordon E., Williams L.M. Enhanced amygdala and medial prefrontal activation during nonconscious processing of fear in posttraumatic stress disorder: an fMRI study. Hum. Brain Mapp. 2008, 29:517-523.
12. Celani G., Battacchi M.W., Arcidiacono L. The understanding of the emotional meaning of facial expressions in people with autism. J. Autism Dev. Disord. 1999, 29:57-66.
13. Conturo T.E., Williams D.L., Smith C.D., Gultepe E., Akbudak E., Minshew N.J. Neuronal fiber pathway abnormalities in autism: an initial MRI diffusion tensor tracking study of hippocampo-fusiform and amygdalo-fusiform pathways. J. Int. Neuropsychol. Soc. 2008, 14:933-946.
14. Critchley H.D., Daly E.M., Bullmore E.T., Williams S.C., Van Amelsvoort T., Robertson D.M., Rowe A., Phillips M., McAlonan G., Howlin P., Murphy D.G. The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 2000, 123(Pt 11):2203-2212.
15. Dalton K.M., Nacewicz B.M., Johnstone T., Schaefer H.S., Gernsbacher M.A., Goldsmith H.H., Alexander A.L., Davidson R.J. Gaze fixation and the neural circuitry of face processing in autism. Nat. Neurosci. 2005, 8:519-526.
16. Dapretto M., Davies M.S., Pfeifer J.H., Scott A.A., Sigman M., Bookheimer S.Y., Iacoboni M. Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat. Neurosci. 2006, 9:28-30.
17. Das P., Kemp A.H., Liddell B.J., Brown K.J., Olivieri G., Peduto A., Gordon E., Williams L.M. Pathways for fear perception: modulation of amygdala activity by thalamo-cortical systems. Neuroimage 2005, 26:141-148.
18. Das P., Kemp A.H., Flynn G., Harris A.W., Liddell B.J., Whitford T.J., Peduto A., Gordon E., Williams L.M. Functional disconnections in the direct and indirect amygdala pathways for fear processing in schizophrenia. Schizophr. Res. 2007, 90:284-294.
19. Dawson G., Webb S.J., McPartland J. Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev. Neuropsychol. 2005, 27:403-424.
20. Duvernoy H.M. The Human Brain Surface, Blood Supply, and Three-Dimensional Sectional Anatomy 1999, Springer-Verlag Wien, New York. Second ed.
21. Eimer M., Holmes A. An ERP study on the time course of emotional face processing. NeuroReport 2002, 13:427-431.
22. Endo T., Shioiri T., Kitamura H., Kimura T., Endo S., Masuzawa N., Someya T. Altered chemical metabolites in the amygdala-hippocampus region contribute to autistic symptoms of autism spectrum disorders. Biol. Psychiatry 2007, 62:1030-1037.
23. Gabis L., Wei H., Azizian A., DeVincent C., Tudorica A., Kesner-Baruch Y., Roche P., Pomeroy J. 1H-magnetic resonance spectroscopy markers of cognitive and language ability in clinical subtypes of autism spectrum disorders. J. Child Neurol. 2008, 23:766-774.
24. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Paus T., Evans A.C., Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999, 2:861-863.
25. Grelotti D.J., Klin A.J., Gauthier I., Skudlarski P., Cohen D.J., Gore J.C., Volkmar F.R., Schultz R.T. fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism. Neuropsychologia 2005, 43:373-385.
26. Hadjikhani N., Joseph R.M., Snyder J., Chabris C.F., Clark J., Steele S., McGrath L., Vangel M., Aharon I., Feczko E., Harris G.J., Tager-Flusberg H. Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces. Neuroimage 2004, 22:1141-1150.
27. Hadjikhani N., Joseph R.M., Snyder J., Tager-Flusberg H. Abnormal activation of the social brain during face perception in autism. Hum. Brain Mapp. 2007, 28(5):441-449.
28. Haith M.M., Bergman T., Moore M.J. Eye contact and face scanning in early infancy. Science 1977, 198:853-855.
29. Hall G.B., West C.D., Szatmari P. Backward masking: evidence of reduced subcortical amygdala engagement in autism. Brain Cogn. 2007, 65:100-106.
30. Hardan A.Y., Girgis R.R., Adams J., Gilbert A.R., Keshavan M.S., Minshew N.J. Abnormal brain size effect on the thalamus in autism. Psychiatry Res. 2006, 147:145-151.
31. Hardan A.Y., Girgis R.R., Adams J., Gilbert A.R., Melhem N.M., Keshavan M.S., Minshew N.J. Brief report: abnormal association between the thalamus and brain size in Asperger's disorder. J. Autism Dev. Disord. 2008, 38:390-394.
32. Hardan A.Y., Minshew N.J., Melhem N.M., Srihari S., Jo B., Bansal R., Keshavan M.S., Stanley J.A. An MRI and proton spectroscopy study of the thalamus in children with autism. Psychiatry Res. 2008, 163:97-105.
33. Haznedar M.M., Buchsbaum M.S., Hazlett E.A., LiCalzi E.M., Cartwright C., Hollander E. Volumetric analysis and three-dimensional glucose metabolic mapping of the striatum and thalamus in patients with autism spectrum disorders. Am. J. Psychiatry 2006, 163:1252-1263.
34. Hobson R.P., Ouston J., Lee A. What's in a face? The case of autism. Br. J. Psychol. 1988, 79(Pt 4):441-453.
35. Honeycutt N.A., Smith P.D., Aylward E., Li Q., Chan M., Barta P.E., Pearlson G.D. Mesial temporal lobe measurements on magnetic resonance imaging scans. Psychiatry Res. 1998, 83:85-94.
36. Hsu M., Yeung-Courchesne R., Courchesne E., Press G.A. Absence of magnetic resonance imaging evidence of pontine abnormality in infantile autism. Arch. Neurol. 1991, 48:1160-1163.
37. Hubl D., Bolte S., Feineis-Matthews S., Lanfermann H., Federspiel A., Strik W., Poustka F., Dierks T. Functional imbalance of visual pathways indicates alternative face processing strategies in autism. Neurology 2003, 61:1232-1237.
38. Humphreys, K., Hasson, U., Avidan, G., Minshew, N., Behrmann, M., 2008. Cortical patterns of category-selective activation for faces, places and objects in adults with autism. 1 (1), 52-63.
39. Ishai A., Pessoa L., Bikle P.C., Ungerleider L.G. Repetition suppression of faces is modulated by emotion. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9827-9832.
40. Janik S.W., Wellens A.R., Goldberg M.L., Dell'osso L.F. Eyes as the center of focus in the visual examination of human faces. Percept. Mot. Skills 1978, 47:857-858.
41. Jenkinson M., Bannister P.R., Brady J.M., Smith S. Improved optimisation for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17:825-841.
42. Johnson M.H. Subcortical face processing. Nat. Rev. Neurosci. 2005, 6:766-774.
43. Jones W., Carr K., Klin A. Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-old toddlers with autism spectrum disorder. Arch. Gen. Psychiatry 2008, 65:946-954.
44. Kamio Y., Wolf J., Fein D. Automatic processing of emotional faces in high-functioning pervasive developmental disorders: An affective priming study. J. Autism Dev. Disord. 2006, 36:155-167.
45. Kleinhans N.M., Richards T., Sterling L., Stegbauer K.C., Mahurin R., Johnson L.C., Greenson J., Dawson G., Aylward E. Abnormal functional connectivity in autism spectrum disorders during face processing. Brain 2008, 131:1000-1012.
46. Klin A., Jones W., Schultz R., Volkmar F., Cohen D. Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Arch. Gen. Psychiatry 2002, 59:809-816.
47. Koshino H., Kana R.K., Keller T.A., Cherkassky V.L., Minshew N.J., Just M.A. fMRI investigation of working memory for faces in autism: visual coding and underconnectivity with frontal areas. Cereb. Cortex 2008, 18(2):289-300.
48. LeDoux J. The Emotional Brain 1996, Simon & Schuster, New York.
49. Liddell B.J., Brown K.J., Kemp A.H., Barton M.J., Das P., Peduto A., Gordon E., Williams L.M. A direct brainstem-amygdala-cortical 'alarm' system for subliminal signals of fear. Neuroimage 2005, 24:235-243.
50. Livingstone M., Hubel D. Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 1988, 240:740-749.
51. Lord C., Rutter M., Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J. Autism Dev. Disord. 1994, 24:659-685.
52. Lord C., Risi S., Lambrecht L., Cook E., Leventhal B., DiLavore P., Pickles A., Rutter M. The Autism Diagnostic Observation Schedule-Generic: a standard measure of social and communication deficits associated with the spectrum of autism. J. Autism Dev. Disord. 2000, 30:205-223.
53. Merigan W.H., Maunsell J.H. How parallel are the primate visual pathways?. Annu. Rev. Neurosci. 1993, 16:369-402.
54. Monk C.S., Telzer E.H., Mogg K., Bradley B.P., Mai X., Louro H.M., Chen G., McClure-Tone E.B., Ernst M., Pine D.S. Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. Arch. Gen. Psychiatry 2008, 65:568-576.
55. Morris J.S., Ohman A., Dolan R.J. A subcortical pathway to the right amygdala mediating "unseen" fear. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:1680-1685.
56. Morris J.P., Pelphrey K.A., McCarthy G. Controlled Scanpath Variation Alters Fusiform Face Activation 2007, 31-38.
57. Morris J.P., Pelphrey K.A., McCarthy G. Face processing without awareness in the right fusiform gyrus. Neuropsychologia 2007, 45:3087-3091.
58. Munson J., Dawson G., Abbott R., Faja S., Webb S.J., Friedman S.D., Shaw D., Artru A., Dager S.R. Amygdalar volume and behavioral development in autism. Arch. Gen. Psychiatry 2006, 63:686-693.
59. Nacewicz B.M., Dalton K.M., Johnstone T., Long M.T., McAuliff E.M., Oakes T.R., Alexander A.L., Davidson R.J. Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Arch. Gen. Psychiatry 2006, 63:1417-1428.
60. Neumann D., Spezio M.L., Piven J., Adolphs R. Looking you in the Mouth: Abnormal Gaze in Autism Resulting from Impaired Top-down Modulation of Visual Attention 2006, 194-202.
61. Osterling J., Dawson G. Early recognition of children with autism: a study of first birthday home videotapes. J. Autism Dev. Disord. 1994, 24:247-257.
62. Osterling J.A., Dawson G., Munson J.A. Early recognition of 1-year-old infants with autism spectrum disorder versus mental retardation. Dev. Psychopathol. 2002, 14:239-251.
63. Otsuka H., Harada M., Mori K., Hisaoka S., Nishitani H. Brain metabolites in the hippocampus-amygdala region and cerebellum in autism: an 1H-MR spectroscopy study. Neuroradiology 1999, 41:517-519.
64. Page L.A., Daly E., Schmitz N., Simmons A., Toal F., Deeley Q., Ambery F., McAlonan G.M., Murphy K.C., Murphy D.G.M. In Vivo 1H-Magnetic Resonance Spectroscopy Study of Amygdala-Hippocampal and Parietal Regions in Autism 2006, 2189-2192.
65. Pelphrey K.A., Morris J.P., McCarthy G. Grasping the intentions of others: the perceived intentionality of an action influences activity in the superior temporal sulcus during social perception. J. Cogn. Neurosci. 2004, 16:1706-1716.
66. Pelphrey K.A., Morris J.P., McCarthy G., Labar K.S. Perception of dynamic changes in facial affect and identity in autism. Soc. Cogn. Affect. Neurosci. 2007, 2:140-149.
67. Pessoa L., Japee S., Ungerleider L.G. Visual awareness and the detection of fearful faces. Emotion 2005, 5:243-247.
68. Pierce K., Redcay E. Fusiform function in children with an autism spectrum disorder is a matter of "who". Biol. Psychiatry 2008, 64:552-560.
69. Pierce K., Muller R.A., Ambrose J., Allen G., Courchesne E. Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. Brain 2001, 124:2059-2073.
70. Pierce K., Haist F., Sedaghat F., Courchesne E. The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain 2004, 127:2703-2716.
71. Piggot J., Kwon H., Mobbs D., Blasey C., Lotspeich L., Menon V., Bookheimer S., Reiss A.L. Emotional attribution in high-functioning individuals with autistic spectrum disorder: a functional imaging study. J. Am. Acad. Child Adolesc. Psychiatry 2004, 43:473-480.
72. Pinkham A.E., Hopfinger J.B., Pelphrey K.A., Piven J., Penn D.L. Neural bases for impaired social cognition in schizophrenia and autism spectrum disorders. Schizophr. Res. 2008, 99:164-175.
73. Pourtois G., Thut G., Grave de Peralta R., Michel C., Vuilleumier P. Two electrophysiological stages of spatial orienting towards fearful faces: early temporo-parietal activation preceding gain control in extrastriate visual cortex. Neuroimage 2005, 26:149-163.
74. Rauch S.L., Whalen P.J., Shin L.M., McInerney S.C., Macklin M.L., Lasko N.B., Orr S.P., Pitman R.K. Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol. Psychiatry 2000, 47:769-776.
75. Schultz R.T. Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int. J. Dev. Neurosci. 2005, 23:125-141.
76. Schultz R.T., Gauthier I., Klin A., Fulbright R.K., Anderson A.W., Volkmar F., Skudlarski P., Lacadie C., Cohen D.J., Gore J.C. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch. Gen. Psychiatry 2000, 57:331-340.
77. Schumann C.M., Amaral D.G. Stereological analysis of amygdala neuron number in autism. J. Neurosci. 2006, 26:7674-7679.
78. Schumann C.M., Hamstra J., Goodlin-Jones B.L., Lotspeich L.J., Kwon H., Buonocore M.H., Lammers C.R., Reiss A.L., Amaral D.G. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J. Neurosci. 2004, 24:6392-6401.
79. Shaw P., Kabani N.J., Lerch J.P., Eckstrand K., Lenroot R., Gogtay N., Greenstein D., Clasen L., Evans A., Rapoport J.L., Giedd J.N., Wise S.P. Neurodevelopmental Trajectories of the Human Cerebral Cortex 2008, 3586-3594.
80. Sheline Y.I., Barch D.M., Donnelly J.M., Ollinger J.M., Snyder A.Z., Mintun M.A. Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol. Psychiatry 2001, 50:651-658.
81. Simion F., Leo I., Turati C., Valenza E., Dalla Barba B. How face specialization emerges in the first months of life. Prog. Brain Res. 2007, 164:169-185.
82. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
83. Sparks B.F., Friedman S.D., Shaw D.W., Aylward E.H., Echelard D., Artru A.A., Maravilla K.R., Giedd J.N., Munson J., Dawson G., Dager S.R. Brain structural abnormalities in young children with autism spectrum disorder. Neurology 2002, 59:184-192.
84. Spezio M.L., Adolphs R., Hurley R.S., Piven J. Analysis of face gaze in autism using "Bubbles". Neuropsychologia 2007, 45:144-151.
85. Sterling L., Dawson G., Webb S., Murias M., Munson J., Panagiotides H., Aylward E. The role of face familiarity in eye tracking of faces by individuals with autism spectrum disorders. J. Autism Dev. Disord. 2008, 38(9):1666-1675.
86. Streit M., Dammers J., Simsek-Kraues S., Brinkmeyer J., Wolwer W., Ioannides A. Time course of regional brain activations during facial emotion recognition in humans. Neurosci. Lett. 2003, 342:101-104.
87. Talairach J., Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain 1988, Thieme Medical Publishers, Inc., New York.
88. Tantam D., Monaghan L., Nicholson H., Stirling J. Autistic children's ability to interpret faces: a research note. J. Child Psychol. Psychiatry 1989, 30:623-630.
89. Tsatsanis K.D., Rourke B.P., Klin A., Volkmar F.R., Cicchetti D., Schultz R.T. Reduced thalamic volume in high-functioning individuals with autism. Biol. Psychiatry 2003, 53:121-129.
90. Vuilleumier P., Armony J.L., Driver J., Dolan R.J. Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat. Neurosci. 2003, 6:624-631.
91. Waiter G.D., Williams J.H., Murray A.D., Gilchrist A., Perrett D.I., Whiten A. A voxel-based investigation of brain structure in male adolescents with autistic spectrum disorder. Neuroimage 2004, 22:619-625.
92. Wang A.T., Dapretto M., Hariri A.R., Sigman M., Bookheimer S.Y. Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. J. Am. Acad. Child Adolesc. Psychiatry 2004, 43:481-490.
93. Wicker B., Fonlupt P., Hubert B., Tardif C., Gepner B., Deruelle C. Abnormal Cerebral Effective Connectivity During Explicit Emotional Processing in Adults with Autism Spectrum Disorder 2008, 135-143.
94. Woolrich M.W., Ripley B.D., Brady M., Smith S.M. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 2001, 14:1370-1386.