Prefrontal social cognition network dysfunction underlying face encoding and social anxiety in fragile X syndrome

NeuroImage

Volumn 43, Issue 3, 2008, Pages 592-604

  Holsen, Laura M ^a   Dalton, Kim M ^a   Johnstone, Tom ^a   Davidson, Richard J ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

Author keywords

Brain function; Face encoding; Fragile X syndrome; Social anxiety; Subsequent memory

Indexed keywords

ADULT; ARTICLE; BRAIN FUNCTION; CLINICAL ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; FACE PROFILE; FEMALE; FRAGILE X SYNDROME; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAZE; HUMAN; MALE; NERVE CELL NECROSIS; PREFRONTAL CORTEX; PRIORITY JOURNAL; SOCIAL PHOBIA; VISUAL DISCRIMINATION;

ADOLESCENT; ANXIETY; BRAIN MAPPING; FACE; FEMALE; FRAGILE X SYNDROME; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; PATTERN RECOGNITION, VISUAL; PREFRONTAL CORTEX; SOCIAL BEHAVIOR; SOCIAL BEHAVIOR DISORDERS;

EID: 54149087431     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2008.08.009     Document Type: Article

References (84)

1. Abitbol M., Menini C., Delezoide A.L., Rhyner T., Vekemans M., and Mallet J. Nucleus basalis magnocellularis and hippocampus are the major sites of FMR-1 expression in the human fetal brain. Nat. Genet. 4 (1993) 147-153
2. Bailey D.B., Mesibov G.B., Hatton D.D., Clark R.D., Roberts J.E., and Mayhew L. Autistic behavior in young boys with fragile X syndrome. J. Autism Dev. Disord. 28 (1998) 499-508
3. Bailey D.B., Roberts J.E., Hooper S.R., Hatton D.D., Mirrett P.L., Roberts J.E., and Schaaf J. Research on fragile X syndrome and autism: implications for the study of genes, environments, and developmental language disorders. In: Rice M.L., and Warren S.F. (Eds). Developmental Language Disorders: From Phenotypes to Etiologies (2004), Lawrence Erlbaum Associates, Inc., Manwah, New Jersey 121-150
4. Baron-Cohen S., Ring H.A., Wheelwright S., Bullmore E.T., Brammer M.J., Simmons A., and Williams S.C. Social intelligence in the normal and autistic brain: an fMRI study. Eur. J. Neurosci. 11 (1999) 1891-1898
5. Beidel D.C., Turner S.M., and Morris T.L. Social Phobia and Anxiety Inventory for Children (1998), Multi-Health Systems, Inc., New York
6. Belmonte M.K., and Bourgeron T. Fragile X syndrome and autism at the intersection of genetic and neural networks. Nat. Neurosci. 9 (2006) 1221-1225
7. Belser R.C., and Sudhalter V. Arousal difficulties in males with fragile X syndrome: a preliminary report. Dev. Brain Dysfunct. 8 (1995) 270-279
8. Bernstein L.J., Beig S., Siegenthaler A.L., and Grady C.L. The effect of encoding strategy on the neural correlates of memory for faces. Neuropsychologia 40 (2002) 86-98
9. Blair R.J., Frith U., Smith N., Abell F., and Cipolotti L. Fractionation of visual memory: agency detection and its impairment in autism. Neuropsychologia 40 (2002) 108-118
10. Boucher J., and Lewis V. Unfamiliar face recognition in relatively able autistic children. J. Child Psychol. Psychiatry 33 (1992) 843-859
11. Brewer J.B., Zhao Z., Desmond J.E., Glover G.H., and Gabrieli J.D. Making memories: brain activity that predicts how well visual experience will be remembered. Science 281 (1998) 1185-1187
12. Cohen I.R. Behavioral profiles of autistic and nonautistic fragile X males. Dev. Brain Dysfunct. 8 (1995) 252-269
13. Cornish K.M., Munir F., and Cross G. Spatial cognition in males with Fragile-X syndrome: evidence for a neuropsychological phenotype. Cortex 35 (1999) 263-271
14. Cornish K.M., Munir F., and Cross G. Differential impact of the FMR-1 full mutation on memory and attention functioning: a neuropsychological perspective. J. Cogn. Neurosci. 13 (2001) 144-150
15. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29 (1996) 162-173
16. Crowe S.F., and Hay D.A. Neuropsychological dimensions of the fragile X syndrome: support for a non-dominant hemisphere dysfunction hypothesis. Neuropsychologia 28 (1990) 9-16
17. Dalton K.M., Nacewicz B.M., Johnstone T., Schaefer H.S., Gernsbacher M.A., Goldsmith H.H., Alexander A.L., and Davidson R.J. Gaze fixation and the neural circuitry of face processing in autism. Nat. Neurosci. 8 (2005) 519-526
18. Dalton, K.M., Holsen, L.M., Abbeduto, L.L., Davidson, R.J., in press. Brain function and gaze-fixation during facial emotion processing in fragile-X and autism. Autism Research.
19. de Gelder B., Vroomen J., and vanDerHeide L. Face recognition and lip-reading in autism. Eur. J. Cogn. Psychol. 3 (1991) 69-86
20. Dolcos F., LaBar K.S., and Cabeza R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 42 (2004) 855-863
21. Dubois S., Rossion B., Schiltz C., Bodart J.M., Michel C., Bruyer R., and Crommelinck M. Effect of familiarity on the processing of human faces. NeuroImage 9 (1999) 278-289
22. Erk S., Martin S., and Walter H. Emotional context during encoding of neutral items modulates brain activation not only during encoding but also during recognition. NeuroImage 26 (2005) 829-838
23. Fletcher P.C., and Henson R.N. Frontal lobes and human memory: insights from functional neuroimaging. Brain 124 (2001) 849-881
24. Freund L.S., and Reiss A.L. Cognitive profiles associated with the fra(X) syndrome in males and females. Am. J. Med. Genet. 38 (1991) 542-547
25. Freund L.S., Reiss A.L., and Abrams M.T. Psychiatric disorders associated with fragile X in the young female. Pediatrics 91 (1993) 321-329
26. Garrett A.S., Menon V., MacKenzie K., and Reiss A.L. Here's looking at you, kid: neural systems underlying face and gaze processing in fragile X syndrome. Arch. Gen. Psychiatry 61 (2004) 281-288
27. Gepner B., de Gelder B., and de Schonen S. Face processing in autistics: evidence for a generalised deficit?. Child Neuropsychol. 2 (1996) 123-139
28. Gilboa A. Autobiographical and episodic memory - one and the same? Evidence from prefrontal activation in neuroimaging studies. Neuropsychologia 42 (2004) 1336-1349
29. Glutting J., Adams W., and Sheslow D. Wide Range Intelligence Test (2000), Wide Range, Wilmington, Delaware
30. Grabner R.H., Ansari D., Reishofer G., Stern E., Ebner F., and Neuper C. Individual differences in mathematical competence predict parietal brain activation during mental calculation. NeuroImage 38 (2007) 346-356
31. Green D.W., and Swets J.A. Signal Detection Theory and Psychophysics (1966), Wiley, New York
32. Greicius M.D., Boyett-Anderson J.M., Menon V., and Reiss A.L. Reduced basal forebrain and hippocampal activation during memory encoding in girls with fragile X syndrome. NeuroReport 15 (2004) 1579-1583
33. Hagerman R.J., and Sobesky W.E. Psychopathology in fragile X syndrome. Am. J. Orthopsychiatr. 59 (1989) 142-152
34. Hagerman R.J., Jackson A.W., Levitas A., Rimland B., and Braden M. An analysis of autism in fifty males with the fragile X syndrome. Am. J. Med. Genet. 23 (1986) 359-374
35. Hagerman R.J., Jackson C., Amiri K., Silverman A.C., O'Connor R., and Sobesky W. Girls with fragile X syndrome: physical and neurocognitive status and outcome. Pediatrics 89 (1992) 395-400
36. Hall S., DeBernardis M., and Reiss A. Social escape behaviors in children with fragile X syndrome. J. Autism Dev. Disord. 36 (2006) 935-947
37. Harvey P.O., Fossati P., and Lepage M. Modulation of memory formation by stimulus content: specific role of the medial prefrontal cortex in the successful encoding of social pictures. J. Cogn. Neurosci. 19 (2007) 351-362
38. Haxby J.V., Ungerleider L.G., Horwitz B., Maisog J.M., Rapoport S.I., and Grady C.L. Face encoding and recognition in the human brain. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 922-927
39. Hessl D., Glaser B., Dyer-Friedman J., Blasey C., Hastie T., Gunnar M., and Reiss A.L. Cortisol and behavior in fragile X syndrome. Psychoneuroendocrinology 27 (2006) 855-872
40. Hessl D., Rivera S., Koldewyn K., Cordeiro L., Adams J., Tassone F., Hagerman P.J., and Hagerman R.J. Amygdala dysfunction in men with the fragile X premutation. Brain 130 (2007) 404-416
41. Hinds H.L., Ashley C.T., Sutcliffe J.S., Nelson D.L., Warren S.T., Housman D.E., and Schalling M. Tissue specific expression of FMR-1 provides evidence for a functional role in fragile X syndrome. Nat. Genet. 3 (1993) 36-43
42. Hoeft F., Hernandez A., Parthasarathy S., Watson C.L., Hall S.S., and Reiss A.L. Fronto-striatal dysfunction and potential compensatory mechanisms in male adolescents with fragile X syndrome. Hum. Brain Mapp. 28 (2007) 543-554
43. Humphries C., Binder J.R., Medler D.A., and Liebenthal E. Time course of semantic processes during sentence comprehension: an fMRI study. NeuroImage 36 (2007) 924-932
44. Johnstone T., Ores Walsh K.S., Greischar L.L., Alexander A.L., Fox A.S., Davidson R.J., and Oakes T.R. Motion correction and the use of motion covariates in multiple-subject fMRI analysis. Hum. Brain Mapp. 27 (2006) 779-788
45. Kates W.R., Abrams M.T., Kaufmann W.E., Breiter S.N., and Reiss A.L. Reliability and validity of MRI measurement of the amygdala and hippocampus in children with fragile X syndrome. Psychiatry Res. 75 (1997) 31-48
46. Kau A.S.M., Tierney E., Bukelis I., Stump M.H., Kates W.R., Trescher W.H., and Kaufmann W.E. Social behavior profile in young males with fragile X syndrome: characteristics and specificity. Am. J. Med. Genet. 126 (2004) 9-17
47. Kensington E.A., and Schacter D.L. Amygdala activity is associated with successful encoding of item, but not source, information for positive and negative information. J. Neurosci. 26 (2006) 2564-2570
48. Klin A., Sparrow S.S., de Bildt A., Cicchetti D.V., Cohen D.J., and Volkmar F.R. A normed study of face recognition in autism and related disorders. J. Autism Dev. Disord. 29 (1999) 499-508
49. LaBar K.S., and Cabeza R. Cognitive neuroscience of emotional memory. Nat. Rev. Neurosci. 7 (2006) 54-64
50. Lesniak-Karpiak K., Mazzocco M.M.M., and Ross J.L. Behavioral assessment of social anxiety in females with Turner or fragile X syndrome. J. Autism Dev. Disord. 33 (2003) 55-67
51. Lewis P., Abbeduto L., Murphy M., Richmond E., Giles N., Bruno L., and Schroeder S. Cognitive, language and social-cognitive skills of individuals with fragile X syndrome with and without autism. J. Intellect. Disabil. Res. 50 (2006) 532-545
52. Lord C., Rutter M., and LeCouteur 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. 24 (1994) 659-685
53. Lundqvist D., Flykt A., and Ohmen A. Karolinska Directed Emotional Faces (1998), Karolinska Hospital Department of Neurosciences, Stockholm
54. Maes B., Fryns J.P., VanWalleghem M., and VandenBerghe H. Cognitive functioning and information processing of adult mentally retarded men with fragile-X syndrome. Am. J. Med. Genet. 50 (1994) 190-200
55. Mason M.F., Banfield J.F., and Macrae C.N. Thinking about actions: the neural substrates of person knowledge. Cereb. Cortex 14 (2004) 209-214
56. Mazzocco M.M.M., Kates W.R., Baumgardner T.L., Freund L.S., and Reiss A.L. Autistic behaviors among girls with fragile X syndrome. J. Autism Dev. Disord. 27 (1997) 415-435
57. Menon V., Leroux J., White C.D., and Reiss A.L. Frontostriatal deficits in fragile X syndrome: relation to FMR1 gene expression. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 3615-3620
58. Mitchell J.P., Macrae C.N., and Banaji M.R. Encoding-specific effects of social cognition on the neural correlates of subsequent memory. J. Neurosci. 24 (2004) 4912-4917
59. Mort D.J., Perry R.J., Mannan S.K., Hodgson T.L., Anderson E., Quest R., McRobbie D., McBride A., Husain M., and Kennard C. Differential cortical activation during voluntary and reflexive saccades in man. NeuroImage 18 (2003) 231-246
60. Munir F., Cornish K.M., and Wilding J. Nature of the working memory deficit in fragile-X syndrome. Brain Cogn. 44 (2000) 387-401
61. Murphy M.M., Abbeduto L., Schroeder S., and Serlin R. Contribution of social and information-processing factors to eye-gaze avoidance in fragile X syndrome. Am. J. Ment. Retard. 112 (2007) 349-360
62. Paller K.A., and Wagner A.D. Observing the transformation of experience into memory. Trends Cogn. Sci. 6 (2002) 93-102
63. Phelps E.A. Emotion and cognition: insights from studies of the human amygdala. Ann. Rev. Psychol. 57 (2006) 27-53
64. Phinney E., Pennington B.F., Olson R., Filley C.M., and Filipek P.A. Brain structure correlates of component reading processes: implications for reading disability. Cortex 43 (2007) 777-791
65. Platek S.M., Loughead J.W., Gur R.C., Busch S., Ruparel K., Phend N., Panyavin I.S., and Langleben D.D. Neural substrates for functionally discriminating self-face from personally familiar faces. Hum. Brain Mapp. 2 (2006) 91-98
66. Reiss A.L., and Dant C.C. The behavioral neurogenetics of fragile X syndrome: analyzing gene-brain-behavior relationships in child developmental psychopathologies. Dev. Psychopathol. 15 (2003) 927-968
67. Reiss A.L., and Freund L. Behavioral phenotype of fragile X syndrome: DSM-III-R autistic behavior in male children. Am. J. Med. Genet. 43 (1992) 35-46
68. Reiss A.L., Lee J., and Freund L. Neuroanatomy of fragile X syndrome: the temporal lobe. Neurology 44 (1994) 1317-1324
69. Richardson M.P., Strange B.A., and Dolan R.J. Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nat. Neurosci. 3 (2004) 278-285
70. Rivera S.M., Menon V., White C.D., Glaser B., and Reiss A.L. Functional brain activation during arithmetic processing in females with fragile X Syndrome is related to FMR1 protein expression. Hum. Brain Mapp. 16 (2002) 206-218
71. Rogers S.J., Wehner E.A., and Hagerman R.J. The behavioral phenotype in fragile X: symptoms of autism in very young children with fragile X syndrome, idiopathic autism, and other developmental disorders. J. Dev. Behav. Pediatr. 22 (2001) 409-417
72. Rutter M.A., Bailey A., and Lord C. Social Communication Questionnaire (2003), Western Psychological Services, Los Angeles
73. Sergerie K., Lepage M., and Armony J.L. A face to remember: emotional expression modulates prefrontal activity during memory formation. NeuroImage 24 (2005) 580-585
74. Sergerie K., Lepage M., and Armony J.L. A process-specific functional dissociation of the amygdala in emotional memory. J. Cogn. Neurosci. 18 (2006) 1359-1367
75. Smith A.P.R., Stephan K.E., Rugg M.D., and Dolan R.J. Task and content modulate amygdala-hippocampal connectivity in emotional retrieval. Neuron 49 (2006) 631-638
76. Talairach J., and Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging (1988), Thieme Medical, New York
77. Tamm L., Menon V., Johnston C.K., Hessl D.R., and Reiss A.L. fMRI study of cognitive interference processing in females with fragile X syndrome. J. Cogn. Neurosci. 14 (2002) 160-171
78. Turk J. The fragile-X syndrome: on the way to a behavioral phenotype. Br. J. Psychiatry 160 (1992) 24-35
79. Turner S.M., Beidel D.C., and Dancu C.V. Social Phobia and Anxiety Inventory (1996), Multi-Health Systems, Inc., North Tonwanada, New York
80. Uddin L.Q., Kaplan J.T., Molnar-Szakacs I., Zaidel E., and Iacoboni M. Self-face recognition activates a frontoparietal "mirror" network in the right hemisphere: an event-related fMRI study. NeuroImage 25 (2005) 926-935
81. Vogeley K., Bussfeld P., Newen A., Herrmann S., Happe F., Falkai P., Maier W., Shah N.J., Fink G.R., and Zilles K. Mind reading: neural mechanisms of theory of mind and self-perspective. NeuroImage 14 (2001) 170-181
82. Wegner D.M., and Bargh J.A. Control and automaticity in social life. In: Gilbert D.T., Fiske S.T., and Lindzey G. (Eds). The Handbook of Social Psychology (1998), McGraw-Hill, New York 226-296
83. Williams D.L., Goldstein G., and Minshew N.J. Impaired memory for faces and social scenes in autism: clinical implications of memory dysfunction. Arch. Clin. Neuropsychol. 20 (2005) 1-15
84. Wolff P.H., Gardner J., Paccia J., and Lappen J. The greeting behavior in fragile X males. Am. J. Ment. Retard. 93 (1989) 406-411