Elevated amygdala response to faces and gaze aversion in autism spectrum disorder

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 1, 2014, Pages 106-117

  Tottenham, Nim ^a,b   Hertzig, Margaret E ^b   Gillespie Lynch, Kristen ^a,c   Gilhooly, Tara ^d   Millner, Alexander J ^e   Casey, B J ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d ST JOHN'S UNIVERSITY   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

Amygdala; Autism spectrum disorders; Eye tracking; Face expressions; Fmri

Indexed keywords

ADOLESCENT; ADULT; AMYGDALOID NUCLEUS; ARTICLE; ATTENTION DEFICIT DISORDER; AUTISM; AUTISM SPECTRUM DISORDERS; CHILD; ESCAPE BEHAVIOR; EYE FIXATION; EYE-TRACKING; FACE; FACE EXPRESSIONS; FACIAL EXPRESSION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; IMAGE PROCESSING; MALE; PATHOLOGY; PATHOPHYSIOLOGY; PATTERN RECOGNITION; PHOTOSTIMULATION; PHYSIOLOGY; REACTION TIME; VASCULARIZATION; YOUNG ADULT;

AMYGDALA; AUTISM SPECTRUM DISORDERS; EYE-TRACKING; FACE EXPRESSIONS; FMRI;

ADOLESCENT; ADULT; AMYGDALA; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; ESCAPE REACTION; FACE; FACIAL EXPRESSION; FEMALE; FIXATION, OCULAR; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; REACTION TIME; YOUNG ADULT;

EID: 84886419638     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst050     Document Type: Article

References (90)

1. Adolphs, R., Sears, L., Piven, J. (2001). Abnormal processing of social information from faces in autism. Journal of Cognitive Neuroscience, 13(2), 232-40.
2. Adolphs, R., Tranel, D., Damasio, H., Damasio, A.R. (1995). Fear and the human amygdala. The Journal of Neuroscience, 15(9), 5879-91.
3. Ashwin, C., Baron-Cohen, S., Wheelwright, S., O'Riordan, M., Bullmore, E.T. (2007). Differential activation of the amygdala and the 'social brain' during fearful face-processing in Asperger Syndrome. Neuropsychologia, 45(1), 2-14.
4. Ashwin, C., Ricciardelli, P., Baron-Cohen, S. (2009). Positive and negative gaze perception in autism spectrum conditions. Social Neuroscience, 4(2), 153-64.
5. Aylward, E.H., Minshew, N.J., Goldstein, G., et al. (1999). MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology, 53(9), 2145-50.
6. Baron, R.M., Kenny, D.A. (1986). The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology, 51(6), 1173-82.
7. Baron-Cohen, S., Ring, H.A., Bullmore, E.T., et al. (2000). The amygdala theory of autism. Neuroscience and Biobehavioral Review, 24(3), 355-64.
8. Baron-Cohen, S., Wheelwright, S., Jolliffe, T. (1997). Is there a "language of the eyes"? Evidence from normal adults and adults with autism or Asperger syndrome. Visual Cognition, 4, 311-31.
9. Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., Clubley, E. (2001). The autismspectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism Developmental Disorders, 31(1), 5-17.
10. Birmaher, B. (1997). The screen for child anxiety related emotional disorders (SCARED): scale construction and psychometric characteristics. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 545.
11. Bookheimer, S.Y., Wang, A.T., Scott, A., Sigman, M., Dapretto, M. (2008). Frontal contributions to face processing differences in autism: evidence from fMRI of inverted face processing. Journal of International Neuropsychological Society, 14(6), 922-32.
12. Bormann-Kischkel, C., Vilsmeier, M., Baude, B. (1995). The development of emotional concepts in autism. Journal of child psychology and psychiatry, and allied disciplines, 36(7), 1243-59.
13. Breiter, H., Etcoff, N.L., Whalen, P.J., et al. (1996). Response and habituation of the human amygdala during visual processing of facial expression. Neuron, 17, 875-87.
14. Carver, L.J., Dawson, G. (2002). Development and neural bases of face recognition in autism. Molecular Psychiatry, 7(Suppl. 2), S18-20.
15. Corbett, B.A., Carmean, V., Ravizza, S., et al. (2009). A functional and structural study of emotion and face processing in children with autism. Psychiatry Research, 173(3), 196-205.
16. Cox, R.W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computations in Biomedical Research, 29, 162-73.
17. Dalton, K.M., Nacewicz, B.M., Johnstone, T., et al. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8(4), 519-26.
18. Davis, M., Whalen, P.J. (2001). The amygdala: vigilance and emotion. Molecular Psychiatry, 6(1), 13-34.
19. Dawson, G., Webb, S.J., McPartland, J. (2005). Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Developmental Neuropsychology, 27(3), 403-24.
20. Dichter, G.S., Richey, J.A., Rittenberg, A.M., Sabatino, A., Bodfish, J.W. (2012). Reward circuitry function in autism during face anticipation and outcomes. Journal of Autism and Developmental Disorders, 42(2), 147-60.
21. DSM-IV. (1994). Diagnostic and Statistical Manual of Mental Disorders. Washington, DC: American Psychiatric Association.
22. Duerden, E.G., Oatley, H.K., Mak-Fan, K.M., et al. (2012). Risk factors associated with selfinjurious behaviors in children and adolescents with autism spectrum disorders. Journal of Autism and Developmental Disorders, 42(11), 2460-70.
23. Dunn, L.M., Dunn, L.M. (1997). Peabody Picture Vocabulary Test, 3rd edn. Circle Pines, MN: American Guidance Service.
24. Ferrara, C., Hill, S.D. (1980). The responsiveness of autistic children to the predictability of social and nonsocial toys. Journal of Autism and Developmental Disorders, 10(1), 51-7.
25. Fusar-Poli, P., Placentino, A., Carletti, F., et al. (2009). Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience, 34(6), 418-432.
26. Gee, D.G., Humphreys, K.L., Flannery, J., et al. (2013). A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. Journal of Neuroscience, 33(10), 4584-93.
27. Glover, G.H., Thomason, M.E. (2004). Improved combination of spiral-in/out images for BOLD fMRI. Magnetic Resonance Imaging, 51(4), 863-8.
28. Golan, O., Ashwin, E., Granader, Y., et al. (2010). Enhancing emotion recognition in children with autism spectrum conditions: an intervention using animated vehicles with real emotional faces. Journal of Autism and Developmental Disorders, 40(3), 269-79.
29. Golan, O., Baron-Cohen, S., Hill, J.J., Golan, Y. (2006). The "reading the mind in films" task: complex emotion recognition in adults with and without autism spectrum conditions. Social Neuroscience, 1(2), 111-23.
30. Gomot, M., Belmonte, M.K., Bullmore, E.T., Bernard, F.A., Baron-Cohen, S. (2008). Brain hyper-reactivity to auditory novel targets in children with high-functioning autism. Brain, 131(Pt 9), 2479-88.
31. Hadjikhani, N., Joseph, R.M., Snyder, J., Tager-Flusberg, H. (2007). Abnormal activation of the social brain during face perception in autism. Human Brain Mapping, 28(5), 441-9.
32. Hariri, A.R., Bookheimer, S.Y., Mazziotta, J.C. (2000). Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport, 11(1), 43-8.
33. Holland, P.C., Gallagher, M. (2006). Different roles for amygdala central nucleus and substantia innominata in the surprise-induced enhancement of learning. Journal of Neuroscience, 26(14), 3791-7.
34. Hopkins, I.M., Gower, M.W., Perez, T.A. (2011). Avatar assistant: improving social skills in students with an ASD through a computer-based intervention. Journal of Autism and Developmental Disorders, 41(11), 1543-55.
35. Johnstone, T., Somerville, L.H., Alexander, A.L., et al. (2005). Stability of amygdala BOLD response to fearful faces over multiple scan sessions. Neuroimage, 25(4), 1112-23.
36. Kim, H., Somerville, L.H., Johnstone, T., et al. (2004). Contextual modulation of amygdala responsivity to surprised faces. Journal of Cognitive Neuroscience, 16(10), 1730-45.
37. Kirchner, J.C., Hatri, A., Heekeren, H.R., Dziobek, I. (2011). Autistic symptomatology, face processing abilities, and eye fixation patterns. Journal of Autism and Developmental Disorders, 41(2), 158-67.
38. Kleinhans, N.M., Johnson, L.C., Richards, T., et al. (2009). Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. American Journal of Psychiatry, 166(4), 467-75.
39. Kleinhans, N.M., Richards, T., Johnson, L.C., et al. (2011). fMRI evidence of neural abnormalities in the subcortical face processing system in ASD. Neuroimage, 54(1), 697-704.
40. Kliemann, D., Dziobek, I., Hatri, A., Baudewig, J., Heekeren, H.R. (2012). The role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders. Journal of Neuroscience, 32(28), 9469-76.
41. Kliemann, D., Dziobek, I., Hatri, A., Steimke, R., Heekeren, H.R. (2010). Atypical reflexive gaze patterns on emotional faces in autism spectrum disorders. Journal of Neuroscience, 30(37), 12281-7.
42. Klin, A., Jones, W., Schultz, R., Volkmar, F., Cohen, D. (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59(9), 809-16.
43. Klin, A., Sparrow, S.S., de Bildt, A., Cicchetti, D.V., Cohen, D.J., Volkmar, F.R. (1999). A normed study of face recognition in autism and related disorders. Journal of Autism and Developmental Disorders, 29(6), 499-508.
44. Kuusikko, S., Haapsamo, H., Jansson-Verkasalo, E., et al. (2009). Emotion recognition in children and adolescents with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(6), 938-45.
45. LaBar, K.S., Gatenby, J.C., Gore, J.C., LeDoux, J.E., Phelps, E.A. (1998). Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron, 20, 937-45.
46. Lionello-DeNolf, K.M., Dube, W.V., McIlvane, W.J. (2010). Evaluation of resistance to change under different disrupter conditions in children with autism and severe intellectual disability. Journal of the Experimental Analysis of Behavior, 93(3), 369-83.
47. Lombardo, M.V., Barnes, J.L., Wheelwright, S.J., Baron-Cohen, S. (2007). Self-referential cognition and empathy in autism. PLoS One, 2(9), e883.
48. Lopata, C., Thomeer, M.L., Volker, M.A., et al. (2010). RCT of a manualized social treatment for high-functioning autism spectrum disorders. Journal of Autism and Developmental Disorders, 40(11), 1297-310.
49. Lord, C., Risi, S., Lambrecht, L., et al. (2000). The autism diagnostic observation schedulegeneric: a standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205-23.
50. Mathersul, D., McDonald, S., Rushby, J.A. (2013). Automatic facial responses to affective stimuli in high-functioning adults with autism spectrum disorder. Physiology & Behavior, 109, 14-22.
51. Minio-Paluello, I., Baron-Cohen, S., Avenanti, A., Walsh, V., Aglioti, S.M. (2009). Absence of embodied empathy during pain observation in Asperger syndrome. Biological Psychiatry, 65(1), 55-62.
52. Monk, C.S., Weng, S.J., Wiggins, J.L., et al. (2010). Neural circuitry of emotional face processing in autism spectrum disorders. Journal of Psychiatry & Neuroscience, 35(2), 105-14.
53. Morita, T., Kosaka, H., Saito, D.N., et al. (2012). Emotional responses associated with selfface processing in individuals with autism spectrum disorders: an fMRI study. Social Neuroscience, 7(3), 223-239.
54. Morris, J.S., deBonis, M., Dolan, R.J. (2002). Human amygdala responses to fearful eyes. Neuroimage, 17(1), 214-22.
55. Mosconi, M.W., Cody-Hazlett, H., Poe, M.D., Gerig, G., Gimpel-Smith, R., Piven, J. (2009). Longitudinal study of amygdala volume and joint attention in 2- to 4-yearold children with autism. Archives of General Psychiatry, 66(5), 509-16.
56. Osterling, J., Dawson, G. (1994). Early recognition of children with autism: a study of first birthday home videotapes. Journal of Autism and Developmental Disorders, 24(3), 247-57.
57. Palmen, S.J., Durston, S., Nederveen, H., van Engeland, H. (2006). No evidence for preferential involvement of medial temporal lobe structures in high-functioning autism. Psychological Medicine, 36(6), 827-34.
58. Pelphrey, K.A., Morris, J.P., McCarthy, G., LaBar, K.S. (2007). Perception of dynamic changes in facial affect and identity in autism. Social Cognitive and Affective Neuroscience, 2(2), 140-9.
59. Perlman, S.B., Hudac, C.M., Pegors, T., Minshew, N.J., Pelphrey, K.A. (2011). Experimental manipulation of face-evoked activity in the fusiform gyrus of individuals with autism. Social Neuroscience, 6(1), 22-30.
60. Phan, K.L., Wager, T., Taylor, S.F., Liberzon, I. (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage, 16(2), 331-348.
61. Pierce, K., Haist, F., Sedaghat, F., Courchesne, E. (2004). The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain, 127(Pt 12), 2703-16.
62. Pierce, K., Redcay, E. (2008). Fusiform function in children with an autism spectrum disorder is a matter of "who". Biological Psychiatry, 64(7), 552-60.
63. Plichta, M.M., Schwarz, A.J., Grimm, O., et al. (2012). Test-retest reliability of evoked BOLD signals from a cognitive-emotive fMRI test battery. Neuroimage, 60(3), 1746-58.
64. Qian, N., Lipkin, R.M. (2011). A learning-style theory for understanding autistic behaviors. Frontiers in Human Neuroscience, 5, 77.
65. Rutherford, M.D., McIntosh, D.N. (2007). Rules versus prototype matching: strategies of perception of emotional facial expressions in the autism spectrum. Journal of Autism and Developmental Disorders, 37(2), 187-96.
66. Samson, A.C., Huber, O., Gross, J.J. (2012). Emotion regulation in Asperger's syndrome and high-functioning autism. Emotion, 12(4), 659-65.
67. Sarinopoulos, I., Grupe, D.W., Mackiewicz, K.L., et al. (2010). Uncertainty during anticipation modulates neural responses to aversion in human insula and amygdala. Cerebral Cortex, 20(4), 929-40.
68. Schultz, R.T. (2005). Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. International journal of developmental neuroscience: the official journal of the International Society for Developmental Neuroscience, 23(2-3), 125-41.
69. Schumann, C.M., Barnes, C.C., Lord, C., Courchesne, E. (2009). Amygdala enlargement in toddlers with autism related to severity of social and communication impairments. Biological Psychiatry, 66(10), 942-9.
70. Schumann, C.M., Hamstra, J., Goodlin-Jones, B.L., et al. (2004). The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. Journal of Neuroscience, 24(28), 6392-401.
71. Schwarzer, G., Huber, S., Dümmler, T. (2005). Gaze behavior in analytical and holistic face processing. Memory & Cognition, 33(2), 344-54.
72. Silver, M., Oakes, P. (2001). Evaluation of a new computer intervention to teach people with autism or Asperger syndrome to recognize and predict emotions in others. Autism, 5(3), 299-316.
73. Sobel, M.E. (1982). Asymptotic intervals for indirect effects in structural equations models. In: Leinhart, S., editor. Sociological methodology. San Francisco: Jossey-Bass, pp. 290-312.
74. Solomon, M., Goodlin-Jones, B.L., Anders, T.F. (2004). A social adjustment enhancement intervention for high functioning autism, Asperger's syndrome, and pervasive developmental disorder NOS. Journal of Autism and Developmental Disorders, 34(6), 649-68.
75. Spielberger, C.D., Gorsuch, R.L., Lushene, R., Vagg, P.R., Jacobs, G.A. (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.
76. Strauss, M.M., Makris, N., Aharon, I., et al. (2005). fMRI of sensitization to angry faces. Neuroimage, 26(2), 389-413.
77. Swartz, J.R., Wiggins, J.L., Carrasco, M., Lord, C., Monk, C.S. (2013). Amygdala habituation and prefrontal functional connectivity in youth with autism spectrum disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 52(1), 84-93.
78. Talairach, J., Tournoux, P. (1988). Co-planar Stereotaxic Atlas of the Human Brain. New York: Thieme.
79. Tanaka, J.W., Wolf, J.M., Klaiman, C., et al. (2012). The perception and identification of facial emotions in individuals with autism spectrum disorders using the Let's Face It! Emotion Skills Battery. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 53(12), 1259-67.
80. Thomas, K.M., Drevets, W.C., Whalen, P.J., et al. (2001). Amygdala response to facial expressions in children and adults. Biological Psychiatry, 49(4), 309-16.
81. Todd, R.M., Cunningham, W.A., Anderson, A.K., Thompson, E. (2012). Affect-biased attention as emotion regulation. Trends in Cognitive Science, 16(7), 365-72.
82. Tottenham, N., Hare, T.A., et al. (2009a). A developmental perspective on human amygdala function. In: Phelps, E., Whalen, P., editors. The Human Amygdala. New York: Guilford Press, pp. 107-117.
83. Tottenham, N., Tanaka, J.W., Leon, A.C., et al. (2009b). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168(3), 242-9.
84. van den Bulk, B.G., Koolschijn, P.C., Meens, P.H., et al. (2013). How stable is activation in the amygdala and prefrontal cortex in adolescence? A study of emotional face processing across three measurements. Developmental Cognitive Neuroscience, 4, 65-76.
85. Wechsler, D. (1999). The Wechsler Abbreviated Scale of Intelligence. New York: The Psychological Corporation.
86. Welchew, D.E., Ashwin, C., Berkouk, K., et al. (2005). Functional disconnectivity of the medial temporal lobe in Asperger's syndrome. Biological Psychiatry, 57(9), 991-8.
87. Weng, S.J., Carrasco, M., Swartz, J.R., et al. (2011). Neural activation to emotional faces in adolescents with autism spectrum disorders. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 52(3), 296-305.
88. Whalen, P.J. (1998). Fear, vigilance, and ambiguity: initial neuroimaing studies of the human amygdala. Current Directions in Psychological Science, 7(6), 177-88.
89. Woodbury-Smith, M.R., Robinson, J., Wheelwright, S., Baron-Cohen, S. (2005). Screening adults for Asperger Syndrome using the AQ: a preliminary study of its diagnostic validity in clinical practice. Journal of Autism and Developmental Disorders, 35(3), 331-5.
90. Yang, T.T., Menon, V., Eliez, S., et al. (2002). Amygdalar activation associated with positive and negative facial expressions. Neuroreport, 13(14), 1737-41.