Aberrant neurocognitive processing of fear in young girls with turner syndrome

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 3, 2014, Pages 255-264

  Hong, David S ^a   Bray, Signe ^a,b,c   Haas, Brian W ^a   Hoeft, Fumiko ^a,d   Reiss, Allan L ^a,e  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anterior cingulate; Emotion; Fear processing; Turner syndrome

Indexed keywords

ADOLESCENT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; CHILD; COGNITION; EMOTION; FACE; FEAR; FEAR PROCESSING; FEMALE; HUMAN; IMAGE PROCESSING; MALE; METHODOLOGY; PATHOPHYSIOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; PREFRONTAL CORTEX; PSYCHOLOGICAL ASPECT; TURNER SYNDROME;

ANTERIOR CINGULATE; EMOTION; FEAR PROCESSING; TURNER SYNDROME;

ADOLESCENT; AMYGDALA; CHILD; COGNITION; FACE; FEAR; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; PHOTIC STIMULATION; PREFRONTAL CORTEX; TURNER SYNDROME;

EID: 84895100758     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nss133     Document Type: Article

References (93)

1. Adolphs, R., Gosselin, F., Buchanan, T.W., Tranel, D., Schyns, P., Damasio, A.R. (2005). A mechanism for impaired fear recognition after amygdala damage. Nature, 433, 68-72.
2. Bakalov, V.K., Bondy, C.A. (2008). Fracture risk and bone mineral density in Turner syndrome. Reviews in Endocrine & Metabolic Disorders, 9, 145-51.
3. Bar, M., Kassam, K.S., Ghuman, A.S., et al. (2006). Top-down facilitation of visual recognition. Proceedings of the National Academy of Sciences of the United States of America, 103, 449-54.
4. Batty, M., Taylor, M.J. (2006). The development of emotional face processing during childhood. Developmental science, 9, 207-20.
5. Beckmann, M., Johansen-Berg, H., Rushworth, M.F. (2009). Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. Journal of Neuroscience, 29, 1175-90.
6. Blakemore, S.J., Burnett, S., Dahl, R.E. (2010). The role of puberty in the developing adolescent brain. Human Brain Mapping, 31, 926-33.
7. Bray, S., Dunkin, B., Hong, D.S., Reiss, A.L. (2011). Reduced functional connectivity during working memory in Turner syndrome. Cerebral Cortex, 21, 2471-81.
8. Brooks-Gunn, J., Warren, M.P., Rosso, J., Gargiulo, J. (1987). Validity of self-report measures of girls' pubertal status. Child development, 58, 829-41.
9. Brotman, M.A., Rich, B.A., Guyer, A.E., et al. (2010). Amygdala activation during emotion processing of neutral faces in children with severe mood dysregulation versus ADHD or bipolar disorder. The American Journal of Psychiatry, 167, 61-9.
10. Bush, G., Luu, P., Posner, M.I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences, 4, 215-22.
11. Bush, G., Vogt, B.A., Holmes, J., et al. (2002). Dorsal anterior cingulate cortex: a role in reward-based decision making. Proceedings of the National Academy of Sciences of the United States of America, 99, 523-8.
12. Campbell, R., Elgar, K., Kuntsi, J., et al. (2002). The classification of 'fear' from faces is associated with face recognition skill in women. Neuropsychologia, 40, 575-84.
13. Casey, B.J., Giedd, J.N., Thomas, K.M. (2000). Structural and functional brain development and its relation to cognitive development. Biological psychology, 54, 241-57.
14. Chen, C.M., Lakatos, P., Shah, A.S., et al. (2007). Functional anatomy and interaction of fast and slow visual pathways in macaque monkeys. Cerebral Cortex, 17, 1561-9.
15. Cooney, R.E., Atlas, L.Y., Joormann, J., Eugene, F., Gotlib, I.H. (2006). Amygdala activation in the processing of neutral faces in social anxiety disorder: is neutral really neutral? Psychiatry Research, 148, 55-9.
16. Corden, B., Critchley, H.D., Skuse, D., Dolan, R.J. (2006). Fear recognition ability predicts differences in social cognitive and neural functioning in men. Journal of Cognitive Neuroscience, 18, 889-97.
17. Derntl, B., Finkelmeyer, A., Eickhoff, S., et al. (2010). Multidimensional assessment of empathic abilities: neural correlates and gender differences. Psychoneuroendocrinology, 35, 67-82.
18. Durand, K., Gallay, M., Seigneuric, A., Robichon, F., Baudouin, J.Y. (2007). The development of facial emotion recognition: the role of configural information. Journal of Experimental Child Psychology, 97, 14-27.
19. Elgar, K., Campbell, R., Skuse, D. (2002). Are you looking at me? Accuracy in processing line-of-sight in Turner syndrome. Proceedings. Biological sciences/The Royal Society, 269, 2415-22.
20. Ernst, M., Pine, D.S., Hardin, M. (2006). Triadic model of the neurobiology of motivated behavior in adolescence. Psychological Medicine, 36, 299-312.
21. Etkin, A., Egner, T., Kalisch, R. (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences, 15, 85-93.
22. Fichtenholtz, H.M., Dean, H.L., Dillon, D.G., Yamasaki, H., McCarthy, G., LaBar, K.S. (2004). Emotion-attention network interactions during a visual oddball task. Brain Research. Cognitive Brain Research, 20, 67-80.
23. Gamer, M., Buchel, C. (2009). Amygdala activation predicts gaze toward fearful eyes. The Journal of Neuroscience, 29, 9123-6.
24. Gao, X., Maurer, D. (2010). A happy story: developmental changes in children's sensitivity to facial expressions of varying intensities. Journal of Experimental Child Psychology, 107, 67-86.
25. Glover, G.H., Law, C.S. (2001). Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magnetic Resonance in Medicine, 46, 515-22.
26. Gobbini, M.I., Haxby, J.V. (2007). Neural systems for recognition of familiar faces. Neuropsychologia, 45, 32-41.
27. Goldstein, J.M., Seidman, L.J., Horton, N.J., et al. (2001). Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cerebral Cortex, 11, 490-7.
28. Good, C.D., Lawrence, K., Thomas, N.S., et al. (2003). Dosage-sensitive X-linked locus influences the development of amygdala and orbitofrontal cortex, and fear recognition in humans. Brain: A Journal of Neurology, 126, 2431-46.
29. Haas, B.W., Mills, D., Yam, A., Hoeft, F., Bellugi, U., Reiss, A. (2009). Genetic influences on sociability: heightened amygdala reactivity and event-related responses to positive social stimuli in Williams syndrome. Journal of Neuroscience, 29, 1132-9.
30. Haberecht, M.F., Menon, V., Warsofsky, I.S., et al. (2001). Functional neuroanatomy of visuo-spatial working memory in Turner syndrome. Human Brain Mapping, 14, 96-107.
31. Halgren, E., Raij, T., Marinkovic, K., Jousmaki, V., Hari, R. (2000). Cognitive response profile of the human fusiform face area as determined by MEG. Cerebral Cortex, 10, 69-81.
32. Hariri, A.R., Mattay, V.S., Tessitore, A., Fera, F., Weinberger, D.R. (2003). Neocortical modulation of the amygdala response to fearful stimuli. Biological Psychiatry, 53, 494-501.
33. Haxby, J.V., Hoffman, E.A., Gobbini, M.I. (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences, 4, 223-33.
34. Haxby, J.V., Hoffman, E.A., Gobbini, M.I. (2002). Human neural systems for face recognition and social communication. Biological Psychiatry, 51, 59-67.
35. Hederstierna, C., Hultcrantz, M., Rosenhall, U. (2009). A longitudinal study of hearing decline in women with Turner syndrome. Acta Otolaryngol, 129, 1434-41.
36. Henson, R.N., Shallice, T., Gorno-Tempini, M.L., Dolan, R.J. (2002). Face repetition effects in implicit and explicit memory tests as measured by fMRI. Cerebral Cortex, 12, 178-86.
37. Hjerrild, B.E., Mortensen, K.H., Gravholt, C.H. (2008). Turner syndrome and clinical treatment. British Medical Bulletin, 86, 77-93.
38. Hong, D.S., Dunkin, B., Reiss, A.L. (2011). Psychosocial functioning and social cognitive processing in girls with Turner syndrome. Journal of Developmental and Behavioral Pediatrics, 32, 512-20.
39. Kalisch, R. (2009). The functional neuroanatomy of reappraisal: time matters. Neuroscience and Biobehavioral Reviews, 33, 1215-26.
40. Kempton, M.J., Haldane, M., Jogia, J., et al. (2009). The effects of gender and COMT Val158Met polymorphism on fearful facial affect recognition: a fMRI study. The International Journal of Neuropsychopharmacology, 12, 371-81.
41. Kennedy, D.P., Adolphs, R. (2010). Impaired fixation to eyes following amygdala damage arises from abnormal bottom-up attention. Neuropsychologia, 48, 3392-8.
42. Kesler, S.R., Blasey, C.M., Brown, W.E., et al. (2003). Effects of X-monosomy and X-linked imprinting on superior temporal gyrus morphology in Turner syndrome. Biological Psychiatry, 54, 636-46.
43. Kesler, S.R., Menon, V., Reiss, A.L. (2006). Neuro-functional differences associated with arithmetic processing in Turner syndrome. Cerebral Cortex, 16, 849-56.
44. Kim, D.H., Adalsteinsson, E., Glover, G.H., Spielman, D.M. (2002). Regularized higherorder in vivo shimming. Magnetic Resonance in Medicine, 48, 715-22.
45. Krolak-Salmon, P., Henaff, M.A., Vighetto, A., Bertrand, O., Mauguiere, F. (2004). Early amygdala reaction to fear spreading in occipital, temporal, and frontal cortex: a depth electrode ERP study in human. Neuron, 42, 665-76.
46. Kveraga, K., Boshyan, J., Bar, M. (2007). Magnocellular projections as the trigger of topdown facilitation in recognition. The Journal of Neuroscience, 27, 13232-40.
47. Lange, K., Williams, L.M., Young, A.W., et al. (2003). Task instructions modulate neural responses to fearful facial expressions. Biological Psychiatry, 53, 226-32.
48. Lawrence, K., Kuntsi, J., Coleman, M., Campbell, R., Skuse, D. (2003). Face and emotion recognition deficits in Turner syndrome: a possible role for X-linked genes in amygdala development. Neuropsychology, 17, 39-49.
49. Lepage, J., Dunkin, B., Hong, D., Reiss, A. (2011). Contribution of executive functions to visuospatial difficulties in prepubertal girls with Turner syndrome. Developmental Neuropsychology, 36, 988-1002.
50. Liu, L., Ioannides, A.A., Streit, M. (1999). Single trial analysis of neurophysiological correlates of the recognition of complex objects and facial expressions of emotion. Brain Topography, 11, 291-303.
51. Luo, Q., Holroyd, T., Jones, M., Hendler, T., Blair, J. (2007). Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG. NeuroImage, 34, 839-47.
52. Mazzola, F., Seigal, A., MacAskill, A., Corden, B., Lawrence, K., Skuse, D.H. (2006). Eye tracking and fear recognition deficits in Turner syndrome. Social Neuroscience, 1, 259-69.
53. McCauley, E., Kay, T., Ito, J., Treder, R. (1987). The Turner syndrome: cognitive deficits, affective discrimination, and behavior problems. Child Development, 58, 464-73.
54. McClure, E.B., Monk, C.S., Nelson, E.E., et al. (2007). Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Archives of General Psychiatry, 64, 97-106.
55. Mechelli, A., Price, C.J., Friston, K.J., Ishai, A. (2004). Where bottom-up meets top-down: neuronal interactions during perception and imagery. Cerebral Cortex, 14, 1256-65.
56. Mechias, M.L., Etkin, A., Kalisch, R. (2010). A meta-analysis of instructed fear studies: implications for conscious appraisal of threat. NeuroImage, 49, 1760-8.
57. Mobbs, D., Garrett, A.S., Menon, V., Rose, F.E., Bellugi, U., Reiss, A.L. (2004). Anomalous brain activation during face and gaze processing in Williams syndrome. Neurology, 62, 2070-6.
58. Montagne, B., Kessels, R.P., Frigerio, E., de Haan, E.H., Perrett, D.I. (2005). Sex differences in the perception of affective facial expressions: do men really lack emotional sensitivity? Cognitive Processing, 6, 136-41.
59. Morris, J.S., Friston, K.J., Buchel, C., et al. (1998a). A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain: A Journal of Neurology, 121(Pt 1), 47-57.
60. Morris, J.S., Ohman, A., Dolan, R.J. (1998b). Conscious and unconscious emotional learning in the human amygdala. Nature, 393, 467-70.
61. Morris, J.S., Ohman, A., Dolan, R.J. (1999). A subcortical pathway to the right amygdala mediating "unseen" fear. Proceedings of the National Academy of Sciences of the United States of America, 96, 1680-5.
62. Murphy, D.G., Allen, G., Haxby, J.V., et al. (1994). The effects of sex steroids, and the X chromosome, on female brain function: a study of the neuropsychology of adult Turner syndrome. Neuropsychologia, 32, 1309-23.
63. Nelson, E.E., Leibenluft, E., McClure, E.B., Pine, D.S. (2005). The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology. Psychological Medicine, 35, 163-74.
64. Neufang, S., Specht, K., Hausmann, M., et al. (2009). Sex differences and the impact of steroid hormones on the developing human brain. Cerebral Cortex, 19, 464-73.
65. Ochsner, K.N., Gross, J.J. (2005). The cognitive control of emotion. Trends in Cognitive Sciences, 9, 242-9.
66. Ohman, A., Carlsson, K., Lundqvist, D., Ingvar, M. (2007). On the unconscious subcortical origin of human fear. Physiology & Behavior, 92, 180-5.
67. Osterlund, M.K., Keller, E., Hurd, Y.L. (2000). The human forebrain has discrete estrogen receptor alpha messenger RNA expression: high levels in the amygdaloid complex. Neuroscience, 95, 333-42.
68. Paulmann, S., Seifert, S., Kotz, S.A. (2010). Orbito-frontal lesions cause impairment during late but not early emotional prosodic processing. Social Neuroscience, 5, 59-75.
69. Pavuluri, M.N., O'Connor, M.M., Harral, E., Sweeney, J.A. (2007). Affective neural circuitry during facial emotion processing in pediatric bipolar disorder. Biological Psychiatry, 62, 158-67.
70. Phillips, M.L., Drevets, W.C., Rauch, S.L., Lane, R. (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry, 54, 504-14.
71. Phillips, M.L., Ladouceur, C.D., Drevets, W.C. (2008). A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry, 13. 829, 833-57.
72. Robinson, J.L., Laird, A.R., Glahn, D.C., Lovallo, W.R., Fox, P.T. (2010). Metaanalytic connectivity modeling: delineating the functional connectivity of the human amygdala. Human Brain Mapping, 31, 173-84.
73. Romans, S.M., Stefanatos, G., Roeltgen, D.P., Kushner, H., Ross, J.L. (1998). Transition to young adulthood in Ullrich-Turner syndrome: neurodevelopmental changes. American Journal of Medical Genetics, 79, 140-7.
74. Rushworth, M.F., Noonan, M.P., Boorman, E.D., Walton, M.E., Behrens, T.E. (2011). Frontal cortex and reward-guided learning and decision-making. Neuron, 70, 1054-69.
75. Saxe, R., Moran, J.M., Scholz, J., Gabrieli, J. (2006). Overlapping and non-overlapping brain regions for theory of mind and self reflection in individual subjects. Social Cognitive and Affective Neuroscience, 1, 229-34.
76. Schneider, S., Peters, J., Bromberg, U., et al. (2011). Boys do it the right way: sex-dependent amygdala lateralization during face processing in adolescents. NeuroImage, 56, 1847-53.
77. Skuse, D.H., Morris, J.S., Dolan, R.J. (2005). Functional dissociation of amygdala-modulated arousal and cognitive appraisal, in Turner syndrome. Brain: A Journal of Neurology, 128, 2084-96.
78. Stein, J.L., Wiedholz, L.M., Bassett, D.S., et al. (2007). A validated network of effective amygdala connectivity. NeuroImage, 36, 736-45.
79. Suzuki, A., Goh, J.O., Hebrank, A., et al. (2011). Sustained happiness? Lack of repetition suppression in right-ventral visual cortex for happy faces. Social Cognitive and Affective Neuroscience, 6, 434-41.
80. Thayer, J.F., Johnsen, B.H. (2000). Sex differences in judgement of facial affect: a multivariate analysis of recognition errors. Scandinavian Journal of Psychology, 41, 243-6.
81. Thomas, K.M., Drevets, W.C., Whalen, P.J., et al. (2001). Amygdala response to facial expressions in children and adults. Biological Psychiatry, 49, 309-16.
82. Vawter, M.P., Evans, S., Choudary, P., et al. (2004). Gender-specific gene expression in post-mortem human brain: localization to sex chromosomes. Neuropsychopharmacology, 29, 373-84.
83. Vuilleumier, P., Armony, J.L., Driver, J., Dolan, R.J. (2001). Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron, 30, 829-41.
84. Vuilleumier, P., Armony, J.L., Driver, J., Dolan, R.J. (2003). Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nature Neuroscience, 6, 624-31.
85. Vuilleumier, P., Richardson, M.P., Armony, J.L., Driver, J., Dolan, R.J. (2004). Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nature Neuroscience, 7, 1271-8.
86. Waber, D.P. (1979). Neuropsychological aspects of Turner's syndrome. Developmental Medicine and Child Neurology, 21, 58-70.
87. Walton, M.E., Croxson, P.L., Behrens, T.E., Kennerley, S.W., Rushworth, M.F. (2007). Adaptive decision making and value in the anterior cingulate cortex. NeuroImage, 36(Suppl. 2), T142-54.
88. Whalen, P.J., Rauch, S.L., Etcoff, N.L., McInerney, S.C., Lee, M.B., Jenike, M.A. (1998). Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. The Journal of Neuroscience, 18, 411-8.
89. Williams, L.M., Barton, M.J., Kemp, A.H., et al. (2005). Distinct amygdala-autonomic arousal profiles in response to fear signals in healthy males and females. NeuroImage, 28, 618-26.
90. Yamagata, B., Barnea-Goraly, N., Marzelli, M.J., et al. (2012). White matter aberrations in prepubertal estrogen-naive girls with monosomic Turner syndrome. Cerebral Cortex, 22, 2761-8.
91. Yurgelun-Todd, D.A., Killgore, W.D. (2006). Fear-related activity in the prefrontal cortex increases with age during adolescence: a preliminary fMRI study. Neuroscience Letters, 406, 194-9.
92. Ziermans, T., Dumontheil, I., Roggeman, C., et al. (2012). Working memory brain activity and capacity link MAOA polymorphism to aggressive behavior during development. Translational Psychiatry.
93. Zinn, A.R., Kushner, H., Ross, J.L. (2008). EFHC2 SNP rs7055196 is not associated with fear recognition in 45,X Turner syndrome. American Journal of Medical Genetics Part B Neuropsychiatric Genetics, 147B, 507-9.