Attention alters neural responses to evocative faces in behaviorally inhibited adolescents

NeuroImage

Volumn 35, Issue 4, 2007, Pages 1538-1546

  Pérez Edgar, Koraly ^a,b   Roberson Nay, Roxann ^c   Hardin, Michael G ^b,d   Poeth, Kaitlin ^e   Guyer, Amanda E ^b   Nelson, Eric E ^b   McClure, Erin B ^f   Henderson, Heather A ^g   Fox, Nathan A ^d   Pine, Daniel S ^b   Ernst, Monique ^b  

^a GEORGE MASON UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

^e SUNY DOWNSTATE MEDICAL CENTER   (United States)

^f GEORGIA STATE UNIVERSITY   (United States)

^g Department of Biology   (United States)

Author keywords

Amygdala; Anxiety; Attention; Face processing; fMRI; Temperament

Indexed keywords

ADOLESCENT; AMYGDALOID NUCLEUS; ANXIETY DISORDER; ARTICLE; ATTENTION; BEHAVIORAL INHIBITION; CHILD BEHAVIOR; FEAR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; PRIORITY JOURNAL; RISK FACTOR; SCHOOL CHILD; STIMULUS RESPONSE; TASK PERFORMANCE; TEMPERAMENT; UNCERTAINTY;

ADOLESCENT; ANGER; ATTENTION; CHILD; EMOTIONS; FACIAL EXPRESSION; FEAR; FEMALE; HAPPINESS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PERSONALITY; PERSONALITY TESTS; PSYCHIATRIC STATUS RATING SCALES; REACTION TIME; TEMPERAMENT;

EID: 34147108781     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2007.02.006     Document Type: Article

References (61)

1. Amaral D.G. Amygdalohippocampal and amygdalocortical projections in the primate brain. Adv. Exp. Med. Biol. 203 (1986) 3-17
2. Bar-Haim Y., Marshall P.J., Fox N.A., Schorr E.A., and Gordon-Salant S. Mismatch negativity in socially withdrawn children. Biol. Psychiatry 54 (2003) 17-24
3. Baxter M.G., and Murray E.A. The amygdala and reward. Nat. Rev., Neurosci. 3 (2002) 563-573
4. Baxter M.G., Parker A., Lindner C.C., Izquierdo A.D., and Murray E.A. Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex. J. Neurosci. 20 (2000) 4311-4319
5. Britton J.C., Phan K.L., Taylor S.F., Fig L.M., and Liberzon I. Corticolimbic blood flow in posttraumatic stress disorder during script-driven imagery. Biol. Psychiatry 57 (2005) 832-840
6. In: Cairns R.B., Bergman L.R., and Kagan J. (Eds). Methods and Models for Studying the Individual (1998), Sage Publications, Inc., Thousand Oaks, CA, USA
7. Calkins S.D., Fox N.A., and Marshall T.R. Behavioral and physiological antecedents of inhibited and uninhibited behavior. Child Dev. 67 (1996) 523-540
8. Coplan R.J., Rubin K.H., Fox N.A., Calkins S.D., and Stewart S.L. Being alone, playing alone, and acting alone: distinguishing among reticence and passive and active solitude in young children. Child Dev. 65 (1994) 129-137
9. Davis M., and Whalen P.J. The amygdala: vigilance and emotion. Mol. Psychiatry 6 (2001) 13-34
10. Davis M., Walker D.L., and Lee Y. Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex. Philos. Trans. R. Soc. Lond., Ser. B Biol. Sci. 352 (1997) 1675-1687
11. Dugas M.J., Buhr K., and Ladouceur R. The role of intolerance of uncertainty in etiology and maintenance. In: Heimberg R.G., et al. (Ed). Generalized Anxiety Disorder: Advances in Research and Practice (2004), Guilford, New York 143-163
12. Ekman P., and Friesen W.V. Pictures of Facial Affect (1976), Consulting Psychology Press, Palo Alto, CA
13. Fox N.A., Rubin K.H., Calkins S.D., Marshall T.R., Coplan R.J., Porges S.W., Long J.M., and Stewart S. Frontal activation asymmetry and social competence at four years of age. Child Dev. 66 (1995) 1771-1784
14. Fox N.A., Henderson H.A., Rubin K.H., Calkins S.D., and Schmidt L.A. Continuity and discontinuity of behavioral inhibition and exuberance: psychophysiological and behavioral influences across the first four years of life. Child Dev. 72 (2001) 1-21
15. Fox N.A., Henderson H.A., Marshall P.J., Nichols K.E., and Ghera M.M. Behavioral inhibition: linking biology and behavior within a developmental framework. Annu. Rev. Psychol. 56 (2005) 235-262
16. Friston K.J., Holmes A., Poline J.B., Price C.J., and Frith C.D. Detecting activations in PET and fMRI levels of inference and power. NeuroImage 4 (1996) 223-235
17. Garcia Coll C., Kagan J., and Reznick J.S. Behavioral inhibition in young children. Child Dev. 55 (1984) 1005-1019
18. Geisser S., and Greenhouse S.W. An extension of Box's results on the use of the F distribution in multivariate analysis. Ann. Math. Stat. 29 (1958) 885-891
19. Goldsmith H.H., and Lemery K.S. Linking temperamental fearfulness and anxiety symptoms: a behavior-genetic perspective. Biol. Psychiatry 48 (2000) 1199-1209
20. Guyer A.E., Nelson E.E., Perez-Edgar K., Hardin M.G., Roberson-Nay R., Monk C.S., Bjork J.M., Henderson H.A., Pine D.S., Fox N.A., and Ernst M. Striatal function alteration in adolescents characterized by early childhood behavioral inhibition. J. Neurosci. 26 (2006) 6399-6405
21. Hardin M.G., Perez-Edgar K., Guyer A.E., Pine D.S., Fox N.A., and Ernst M. Reward and punishment sensitivity in shy and non-shy adults: relations between social and motivated behavior. Pers. Individ. Differ. 40 (2006) 699-711
22. Hariri A.R., Tessitore A., Mattay V.S., Fera F., and Weinberger D.R. The amygdala response to emotional stimuli: a comparison of faces and scenes. NeuroImage 17 (2002) 317-323
23. Henderson H.A., Marshall P.J., Fox N.A., and Rubin K.H. Psychophysiological and behavioral evidence for varying forms and functions of nonsocial behavior in preschoolers. Child Dev. 75 (2004) 236-250
24. Hirshfeld D.R., Rosenbaum J.F., Biederman J., Bolduc E.A., Faraone S.V., Snidman N., Reznick J.S., and Kagan J. Stable behavioral inhibition and its association with anxiety disorder. J. Am. Acad. Child Adolesc. Psych. 31 (1992) 103-111
25. Holmes A.P., and Friston K.J. Generalisability, random effects and population inference. NeuroImage 7 (1998) S754
26. Kagan J. Temperament and the reactions to unfamiliarity. Child Dev. 68 (1997) 139-143
27. Kagan J. Temperamental contributions to affective and behavioral profiles in childhood. In: Holman S.G., and DiBartolo P.M. (Eds). From Social Anxiety to Social Phobia: Multiple Perspectives (2001), Allyn and Bacon, Needham Heights, MA, USA 216-234
28. Kagan J., and Snidman N. The Long Shadow of Temperament (2004), Belknap Press of Harvard University Press, Cambridge, Massachusetts
29. Kagan J., Reznick J.S., Clarke C., Snidman N., and Garcia-Coll C. Behavioral inhibition to the unfamiliar. Child Dev. 55 (1984) 2212-2225
30. Kagan J., Reznick J.S., Snidman N., Gibbons J., and Johnson M.O. Childhood derivatives of inhibition and lack of inhibition to the unfamiliar. Child Dev. 59 (1988) 1580-1589
31. Kagan J., Reznick J.S., and Gibbons J. Inhibited and uninhibited types of children. Child Dev. 60 (1989) 838-845
32. Kagan J., Snidman N., McManis M., and Woodward S. Temperamental contributions to the affect family of anxiety. Psychiatr. Clin. North Am. 24 (2001) 677-688
33. Kaufman J., Birmaher B., Brent D., Rao U., Flynn C., Moreci P., Williamson D., and Ryan N. Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): initial reliability and validity data. J. Am. Acad. Child Adolesc. Psych. 36 (1997) 980-988
34. Krain A.L., Hefton S., Pine D.S., Ernst M., Castellanos F.X., Klein R.G., and Milham M.P. An fMRI examination of developmental differences in the neural correlates of uncertainty and decision-making. J. Child Psychol. Psychiatry 47 (2006) 1023-1030
35. Marshall P.J., and Stevenson-Hinde J. Behavioral inhibition, heart period, and respiratory sinus arrhythmia in young children. Dev. Psychobiol. 33 (1998) 283-292
36. McClure E.B., Monk C.S., Nelson E.E., Parrish J.M., Adler A., Blair R.J.R., Fromm S.J., Charney D.S., Leibenluft E., Ernst M., and Pine D.S. Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Arch. Gen. Psychiatry 64 (2007) 109-116
37. Monk C.S., McClure E.B., Nelson E.E., Zarahn E., Bilder R.M., Leibenluft E., Charney D.S., Ernst M., and Pine D.S. Adolescent immaturity in attention-related brain engagement to emotional facial expressions. NeuroImage 20 (2003) 420-428
38. Pérez-Edgar K., and Fox N.A. Temperament and anxiety disorders. Child Adolesc. Psychiatr. Clin. N. Am. 14 (2005) 681-706
39. Pessoa L., McKenna M., Gutierrez E., and Ungerleider L.G. Neural processing of emotional faces requires attention. Proc. Natl. Acad. Sci. 99 (2002) 11458-11463
40. Pessoa L., Padmala S., and Morland T. Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation. NeuroImage 28 (2005) 249-255
41. Petrovic P., Ingvar M., Stone-Elander S., Petersson K.M., and Hansson P. A PET activation study of dynamic mechanical allodynia in patients with mononeuropathy. Pain 83 (1999) 459-470
42. Petrovic P., Carlsson K., Petersson K.M., Hansson P., and Ingvar M. Context-dependent deactivation of the amygdala during pain. J. Cogn. Neurosci. 16 (2004) 1289-1301
43. Phan K., Britton J., and Taylor S. Corticolimbic blood flow during nontraumatic emotional processing in posttraumatic stress disorder. Arch. Gen. Psychiatry. (2006) 63
44. Pine D.S. Pathophysiology of childhood anxiety disorders. Biol. Psychiatry 46 (1999) 1556-1566
45. Pine D.S., Klein R.G., Mannuzza S., Moulton J.L., Lissek S., Guarding M., and Woldehawariat G. Face-emotion processing in offspring at risk for panic disorder. J. Am. Acad. Child Adolesc. Psych. 44 (2005) 664-672
46. Rauch S.L., Shin L.M., and Wright C.I. Neuroimaging studies of amygdala function in anxiety disorders. Ann. N. Y. Acad. Sci. 985 (2003) 389-410
47. Reynolds G.D., and Richards J.E. Familiarization, attention, and recognition memory in infancy: an event-related potential and cortical source localization study. Dev. Psychol. 41 (2005) 598-615
48. Rich B.A., Vinton D.T., Roberson-Nay R., Hommer R.E., Berghorst L.H., McClure E.B., Fromm S.J., Pine D.S., and Leibenluft E. Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. Proc. Natl. Acad. Sci. 103 (2006) 8900-8905
49. Roberson-Nay R., McClure E.B., Monk C.S., Nelson E.E., Guyer A.E., Fromm S.J., Charney D.S., Leibenluft E., Blair J., Ernst M., and Pine D.S. Increased amygdala activity during successful memory encoding in adolescent major depressive disorder: an fMRI study. Biol. Psychiatry 60 (2006) 966-973
50. Rosenbaum J.F., Biederman J., Gersten M., Hirshfeld D.R., Meminger S.R., Herman J.B., Kagan J., Reznick J.S., and Snidman N. Behavioral inhibition in children of parents with panic disorder and agoraphobia: a controlled study. Arch. Gen. Psychiatry 45 (1988) 463-470
51. Rubin K.H. The Play Observation Scale (POS) (1989), University of Waterloo
52. Schmidt L.A., and Fox N.A. Conceptual, biological, and behavioral distinctions among different categories of shy children. In: Schmidt L.A., and Schulkin J. (Eds). Extreme Fear, Shyness, and Social Phobia: Origins, Biological Mechanisms, and Clinical Outcomes (1999), Oxford University Press, New York
53. Schmidt L.A., Fox N.A., Rubin K.H., Sternberg E.M., Gold P.W., Smith C.C., and Schulkin J. Behavioral and neuroendocrine responses in shy children. Dev. Psychobiol. 30 (1997) 127-140
54. Schwartz C.E., Wright C.I., Shin L.M., Kagan J., and Rauch S.L. Inhibited and uninhibited infants "grown up": adult amygdalar response to novelty. Science 300 (2003) 1952-1953
55. Shmuel A., Augath M., Oeltermann A., and Logothetis N.K. Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area VI. Nat. Neurosci. 9 (2006) 569-577
56. Szeszko P.R., Robinson D., Alvir J.M., Bilder R.M., Lencz T., Ashtari M., Wu H., and Bogerts B. Orbital frontal and amygdala volume reductions in obsessive-compulsive disorder. Arch. Gen. Psychiatry 56 (1999) 913-919
57. Thomas K.M., Drevets W.C., Dahl R.E., Ryan N.D., Birmaher B., Eccard C.H., Axelson D., Whalen P.J., and Casey B.J. Amygdala response to fearful faces in anxious and depressed children. Arch. Gen. Psychiatry 58 (2001) 1057-1063
58. Whalen P.J. Fear, vigilance, and ambiguity: the initial neuroimaging studies of the human amygdala. Curr. Dir. Psychol. Sci. 7 (1998) 177-188
59. Woodward, S.A., 2002. A longitudinal study of infant temperament and brain processing in childhood. Dissertation Abstracts International: Section B: The Sciences and Engineering. 63, 2093.
60. Worsley K.M., Marrett S., Neelin P., Vandal A.C., Friston K.J., and Evans A.C. A unified statistical approach for determining significant signals in images of cerebral activation. Hum. Brain Mapp. 4 (1996) 58-73
61. Zarahn E., Aguirre G., and D'Esposito M. A trial-based experimental design for fMRI. NeuroImage 6 (1997) 122-138