Neural bases of atypical emotional face processing in autism: A meta-analysis of fMRI studies

World Journal of Biological Psychiatry

Volumn 16, Issue 5, 2015, Pages 291-300

  Aoki, Yuta ^a   Cortese, Samuele ^b,c,d   Tansella, Michele ^e  

^a UNIVERSITY OF TOKYO   (Japan)

^b CAMBRIDGE UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^d NEW YORK UNIVERSITY CHILD STUDY CENTER   (United States)

^e UNIVERSITY OF VERONA   (Italy)

Author keywords

Asperger's syndrome; Autistic disorder; Functional magnetic resonance imaging; Human; Pervasive developmental disorders

Indexed keywords

AMYGDALOID NUCLEUS; ARTICLE; ATYPICAL EMOTIONAL FACE PROCESSING; AUTISM; BASAL GANGLION; BRAIN ANALYSIS; BRAIN REGION; CINGULATE GYRUS; CUNEUS; EMOTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HYPOTHALAMUS; IMAGE PROCESSING; INTELLIGENCE QUOTIENT; MAMMILLARY BODY; META ANALYSIS; PARAHIPPOCAMPAL GYRUS; PRECUNEUS; SYSTEMATIC REVIEW; THALAMUS; BRAIN MAPPING; FACIAL EXPRESSION; FACIAL RECOGNITION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; STATISTICS AND NUMERICAL DATA;

AUTISM SPECTRUM DISORDER; BRAIN MAPPING; FACIAL EXPRESSION; FACIAL RECOGNITION; HUMANS; MAGNETIC RESONANCE IMAGING;

EID: 84938240731     PISSN: 15622975     EISSN: 18141412     Source Type: Journal    
DOI: 10.3109/15622975.2014.957719     Document Type: Article

References (77)

1. Adolphs R. 2008. Fear, faces, and the human amygdala. Curr Opin Neurobiol 18: 166-172.
2. Adolphs R. 2010. Conceptual challenges and directions for social neuroscience. Neuron 65: 752-767.
3. Andrzejewski ME, McKee BL, Baldwin AE, Burns L, Hernandez P. 2013. The clinical relevance of neuroplasticity in corticostriatal networks during operant learning. Neurosci Biobehav Rev 37: 2071-2080.
4. Aoki Y, Inokuchi R, Nakao T, Yamasue H. 2013a. Neural bases of antisocial behavior: A voxel-based meta-analysis. Soc Cogn Affect Neurosci. Online publication.
5. Aoki Y, Inokuchi R, Suwa H, Aoki A. 2013b. Age-related change of neurochemical abnormality in attention-defi cit hyperactivity disorder: A meta-analysis. Neurosci Biobehav Rev 37: 1692-1701.
6. Aoki Y, Abe O, Nippashi Y, Yamasue H. 2013c. Comparison of white matter integrity between autism spectrum disorder subjects and typically developing individuals: A meta-analysis of diffusion tensor imaging tractography studies. Mol Autism 4: 25.
7. Aoki Y, Kasai K, Yamasue H. 2012a. Age-related change in brain metabolite abnormalities in autism: A meta-analysis of proton magnetic resonance spectroscopy studies. Transl Psychiatry 2: E69.
8. Aoki Y, Aoki A, Suwa H. 2012b. Reduction of N-acetylaspartate in the medial prefrontal cortex correlated with symptom severity in obsessive-compulsive disorder: meta-analyses of (1) H-MRS studies. Transl Psychiatry 2: E153.
9. Ashwin C, Baron-Cohen S, Wheelwright S, O'Riordan M, Bullmore E. 2007. Differential activation of the amygdala and the ' social brain ' during fearful face-processing in Asperger Syndrome. Neuropsychologia 45: 2-14.
10. American Psychiatric Association. 2013. Diagnostic and statistical manual of mental disorders. 5th ed. American Psychiatric Publishing.
11. Bellani M, Fornasari L, Chittaro L, Brambilla P. 2011. Virtual reality in autism: state of the art. Epidemiol Psychiatr Sci 20: 235-238.
12. Bolte S, Hubl D, Feineis-Matthews S, Prvulovic D, Dierks T, Poustka F. 2006. Facial affect recognition training in autism: can we animate the fusiform gyrus? Behav Neurosci 120: 211-216.
13. Bora E, Fornito A, Yucel M, Pantelis C. 2011. The effects of gender on grey matter abnormalities in major psychoses: A comparative voxelwise meta-analysis of schizophrenia and bipolar disorder. Psychol Med 11: 1-13.
14. Bornstein AM, Daw ND. 2011. Multiplicity of control in the basal ganglia: computational roles of striatal subregions. Curr Opin Neurobiol 21: 374-380.
15. Brambilla P, Hardan AY, di Nemi SU, Caverzasi E, Soares JC, Perez J, et al. 2004. The functional neuroanatomy of autism. Funct Neurol 19: 9-17.
16. Cauda F, Geda E, Sacco K, D ' Agata F, Duca S, Geminiani G, et al. 2011. Grey matter abnormality in autism spectrum disorder: An activation likelihood estimation meta-analysis study. J Neurol Neurosurg Psychiatry 82: 1304-1313.
17. Celani G, Battacchi MW, Arcidiacono L. 1999. The understanding of the emotional meaning of facial expressions in people with autism. J Autism Dev Disord 29: 57-66.
18. Corbett BA, Carmean V, Ravizza S, Wendelken C, Henry ML, Carter C, et al. 2009. A functional and structural study of emotion and face processing in children with autism. Psychiatry Res 173: 196-205.
19. Cortese S, Kelly C, Chabernaud C, Proal E, Di Martino A, Milham MP, et al. 2012. Toward systems neuroscience of ADHD: A meta-analysis of 55 fMRI studies. Am J Psychiatry 169: 1038-1055.
20. Critchley H, Daly E, Bullmore E, Williams S, Van Amelsvoort T, Robertson D, et al. 2000. The functional neuroanatomy of social behaviour: changes in cerebral blood fl ow when people with autistic disorder process facial expressions. Brain 123: 2203-2212.
21. Dalgleish T. 2004. The emotional brain. Nat Rev Neurosci 5: 583-589.
22. Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, et al. 2005. Gaze fi xation and the neural circuitry of face processing in autism. Nat Neurosci 8: 519-526.
23. Deeley Q, Daly EM, Surguladze S, Page L, Toal F, Robertson D, et al. 2007. An event related functional magnetic resonance imaging study of facial emotion processing in Asperger syndrome. Biol Psychiatry 62: 207-217.
24. Delvecchio G, Sugranyes G, Frangou S. 2013. Evidence of diagnostic specifi city in the neural correlates of facial affect processing in bipolar disorder and schizophrenia: A meta-analysis of functional imaging studies. Psychol Med 43: 553-569.
25. Di Martino A, Ross K, Uddin LQ, Sklar AB, Castellanos FX, Milham MP. 2009. Functional brain correlates of social and nonsocial processes in autism spectrum disorders: An activation likelihood estimation meta-analysis. Biol Psychiatry 65: 63-74.
26. Dickstein DP, Pescosolido MF, Reidy BL, Galvan T, Kim KL, Seymour KE, et al. 2013. Developmental meta-analysis of the functional neural correlates of autism spectrum disorders. J Am Acad Child Adolesc Psychiatry 52: 279-289, e16.
27. Fombonne E. 2003. The prevalence of autism. J Am Med Asoc 289: 87-89.
28. Fusar-Poli P. 2012. Voxel-wise meta-analysis of fMRI studies in patients at clinical high risk for psychosis. J Psychiatry Neurosci 37: 106-112.
29. Gordon I, Vander Wyk BC, Bennett RH, Cordeaux C, Lucas MV, Eilbott JA, et al. 2013. Oxytocin enhances brain function in children with autism. Proc Natl Acad Sci USA 110: 20953-20958.
30. Greimel E, Schulte-Ruther M, Kircher T, Kamp-Becker I, Remschmidt H, Fink GR, et al. 2010. Neural mechanisms of empathy in adolescents with autism spectrum disorder and their fathers. Neuroimage 49: 1055-1065.
31. Happe F, Ronald A, Plomin R. 2006. Time to give up on a single explanation for autism. Nat Neurosci 9: 1218-1220.
32. Harms MB, Martin A, Wallace GL. 2010. Facial emotion recognition in autism spectrum disorders: A review of behavioral and neuroimaging studies. Neuropsychol Rev 20: 290-322.
33. Hart H, Radua J, Mataix-Cols D, Rubia K. 2012. Meta-analysis of fMRI studies of timing in attention-defi cit hyperactivity disorder (ADHD). Neurosci Biobehav Rev 36: 2248-2256.
34. Hart H, Radua J, Nakao T, Mataix-Cols D, Rubia K. 2013. Metaanalysis of functional magnetic resonance imaging studies of inhibition and attention in attention-defi cit/hyperactivity disorder: Exploring task-specifi c, stimulant medication, and age effects. J Am Med Assoc Psychiatry 70: 185-198.
35. Haznedar MM, Buchsbaum MS, Hazlett EA, LiCalzi EM, Cartwright C, Hollander E. 2006. Volumetric analysis and three-dimensional glucose metabolic mapping of the striatum and thalamus in patients with autism spectrum disorders. Am J Psychiatry 163: 1252-1263.
36. Horder J, Lavender T, Mendez MA, O'Gorman R, Daly E, Craig MC, et al. 2013. Reduced subcortical glutamate/ glutamine in adults with autism spectrum disorders: A [(1)H] MRS study. Transl Psychiatry 3: E279.
37. Hubl D, B ö lte S, Feineis-Matthews S, Lanfermann H, Federspiel A, Strik W, et al. 2003. Functional imbalance of visual pathways indicates alternative face processing strategies in autism. Neurology 61: 1232-1237.
38. Ishitobi M, Kosaka H, Omori M, Matsumura Y, Munesue T, Mizukami K, et al. 2011. Differential amygdala response to lower face in patients with autistic spectrum disorders: An fMRI study. Res Autism Spectr Disord 5: 910-919.
39. Kim YS, Leventhal BL, Koh YJ, Fombonne E, Laska E, Lim EC, et al. 2011. Prevalence of autism spectrum disorders in a total population sample. Am J Psychiatry 168: 904-912.
40. Kleinhans NM, Richards T, Johnson LC, Weaver KE, Greenson J, Dawson G, et al. 2011. fMRI evidence of neural abnormalities in the subcortical face processing system in ASD. Neuroimage 54: 697-704.
41. Langen M, Bos D, Noordermeer SD, Nederveen H, van Engeland H, Durston S. 2013. Changes in the development of striatum are involved in repetitive behavior in autism. Biol Psychiatry. Online publication.
42. Langen M, Durston S, Kas MJ, van Engeland H, Staal WG. 2011a. The neurobiology of repetitive behavior: and men. Neurosci Biobehav Rev 35: 356-365.
43. Langen M, Kas MJ, Staal WG, van Engeland H, Durston S. 2011b. The neurobiology of repetitive behavior: of mice. Neurosci Biobehav Rev 35: 345-355.
44. Lemonnier E, Degrez C, Phelep M, Tyzio R, Josse F, Grandgeorge M, et al. 2012. A randomised controlled trial of bumetanide in the treatment of autism in children. Transl Psychiatry 2: E202.
45. Liljeholm M, O'Doherty JP. 2012. Contributions of the striatum to learning, motivation, and performance: An associative account. Trends Cogn Sci 16: 467-475.
46. Lin IF, Kashino M, Ohta H, Yamada T, Tani M, Watanabe H, et al. 2014. The effect of intranasal oxytocin versus placebo treatment on the autonomic responses to human sounds in autism: A single-blind, randomized, placebo-controlled, crossover design study. Mol Autism 5: 20.
47. Lynch CJ, Uddin LQ, Supekar K, Khouzam A, Phillips J, Menon V. 2013. Default mode network in childhood autism: posteromedial cortex heterogeneity and relationship with social defi cits. Biol Psychiatry 74: 212-219.
48. Moher D, Cook DJ, Eastwood S, Olkin I, Rennie D, Stroup DF. 1999. Improving the quality of reports of meta-analyses of randomised controlled trials: The QUOROM statement. Quality of Reporting of Meta-analyses. Lancet 354: 1896-1900.
49. Morita T, Kosaka H, Saito DN, Ishitobi M, Munesue T, Itakura S, et al. 2011. Emotional responses associated with self-face processing in individuals with autism spectrum disorders: An fMRI study. Soc Neurosci 7: 223-239.
50. Nair A, Treiber JM, Shukla DK, Shih P, Muller RA. 2013. Impaired thalamocortical connectivity in autism spectrum disorder: A study of functional and anatomical connectivity. Brain 136: 1942-1955.
51. Nakao T, Radua J, Rubia K, Mataix-Cols D. 2011. Gray matter volume abnormalities in ADHD: voxel-based meta-analysis exploring the effects of age and stimulant medication. Am J Psychiatry 168: 1154-1163.
52. Norbury R, Selvaraj S, Taylor MJ, Harmer C, Cowen PJ. 2010. Increased neural response to fear in patients recovered from depression: A 3T functional magnetic resonance imaging study. Psychol Med 40: 425-432.
53. Pelphrey KA, Carter EJ. 2008. Charting the typical and atypical development of the social brain. Dev Psychopathol 20: 1081-1102.
54. Pelphrey KA, Morris JP, McCarthy G, Labar KS. 2007. Perception of dynamic changes in facial affect and identity in autism. Soc Cogn Affect Neurosci 2: 140-149.
55. Pelphrey KA, Sasson NJ, Reznick JS, Paul G, Goldman BD, Piven J. 2002. Visual scanning of faces in autism. J Autism Deve Disord 32: 249-261.
56. Perlman SB, Hudac CM, Pegors T, Minshew NJ, Pelphrey KA. 2011. Experimental manipulation of face-evoked activity in the fusiform gyrus of individuals with autism. Soc Neurosci 6: 22-30.
57. Peron J, Fruhholz S, Verin M, Grandjean D. 2013. Subthalamic nucleus: A key structure for emotional component synchronization in humans. Neurosci Biobehav Rev 37: 358-373.
58. Philip RC, Dauvermann MR, Whalley HC, Baynham K, Lawrie SM, Stanfi eld AC. 2012. A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders. Neurosci Biobehav Rev 36: 901-942.
59. Radua J, Borgwardt S, Crescini A, Mataix-Cols D, Meyer-Lindenberg A, McGuire PK, et al. 2012. Multimodal meta-analysis of structural and functional brain changes in fi rst episode psychosis and the effects of antipsychotic medication. Neurosci Biobehav Rev 36: 2325-2333.
60. Radua J, Mataix-Cols D. 2009. Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. Br J Psychiatry 195: 393-402.
61. Radua J, Mataix-Cols D, Phillips ML, El-Hage W, Kronhaus DM, Cardoner N, et al. 2012. A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. Eur Psychiatry 27: 605-611.
62. Radua J, van den Heuvel OA, Surguladze S, Mataix-Cols D. 2010. Meta-analytical comparison of voxel-based morphometry studies in obsessive-compulsive disorder vs other anxiety disorders. Arch Gen Psychiatry 67: 701-711.
63. Rahko JS, Paakki JJ, Starck TH, Nikkinen J, Pauls DL, Katsyri JV, et al. 2012. Valence scaling of dynamic facial expressions is altered in high-functioning subjects with autism spectrum disorders: An fMRI study. J Autism Dev Disord 42: 1011-1024.
64. Roland PE, Levin B, Kawashima R, A kerman S. 1993. Threedimensional analysis of clustered voxels in 15O-butanol brain activation images. Human Brain Mapping 1: 3-19.
65. Rudie JD, Hernandez LM, Brown JA, Beck-Pancer D, Colich NL, Gorrindo P, et al. 2012. Autism-associated promoter variant in MET impacts functional and structural brain networks. Neuron 75: 904-915.
66. Sears LL, Vest C, Mohamed S, Bailey J, Ranson BJ, Piven J. 1999. An MRI study of the basal ganglia in autism. Prog Neuropsychopharmacol Biol Psychiatry 23: 613-624.
67. Sigman MD, Kasari C, Kwon JH, Yirmiya N. 1992. Responses to the negative emotions of others by autistic, mentally retarded, and normal children. Child Dev 63: 796-807.
68. Sonuga-Barke EJ1, Brandeis D, Cortese S, Daley D, Ferrin M, Holtmann M et al. 2013. Nonpharmacological interventions for ADHD: systematic review and meta-analyses of randomized controlled trials of dietary and psychological treatments. Am J Psychiatr y 170: 275-289.
69. Tamietto M, de Gelder B. 2010. Neural bases of the non-conscious perception of emotional signals. Nat Rev Neurosci 11: 697-709.
70. Tantam D, Monaghan L, Nicholson H, Stirling J. 1989. Autistic children ' s ability to interpret faces: A research note. J Child Psychol Psychiatry 30: 623-630.
71. Tsatsanis KD, Rourke BP, Klin A, Volkmar FR, Cicchetti D, Schultz RT. 2003. Reduced thalamic volume in high-functioning individuals with autism. Biol Psychiatry 53: 121-129.
72. Via E, Radua J, Cardoner N, Happe F, Mataix-Cols D. 2011. Meta-analysis of gray matter abnormalities in autism spectrum disorder: should Asperger disorder be subsumed under a broader umbrella of autistic spectrum disorder? Arch Gen Psychiatry 68: 409-418.
73. Weigelt S, Koldewyn K, Kanwisher N. 2012. Face identity recognition in autism spectrum disorders: A review of behavioral studies. Neurosci Biobehav Rev 36: 1060-1084.
74. Weng SJ, Carrasco M, Swartz JR, Wiggins JL, Kurapati N, Liberzon I, et al. 2011. Neural activation to emotional faces in adolescents with autism spectrum disorders. J Child Psychol Psychiatry 52: 296-305.
75. Wicker B, Fonlupt P, Hubert B, Tardif C, Gepner B, Deruelle C. 2008. Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Soc Cogn Affect Neurosci 3: 135-143.
76. Yamasue H, Yee JR, Hurlemann R, Rilling JK, Chen FS, Meyer-Lindenberg A, et al. 2012. Integrative approaches utilizing oxytocin to enhance prosocial behavior: from animal and human social behavior to autistic social dysfunction. J Neurosci 32: 14109-14117.
77. Yirmiya N, Sigman MD, Kasari C, Mundy P. 1992. Empathy and cognition in high-functioning children with autism. Child Dev 63: 150-160.