A preliminary study of the neural mechanisms of frustration in pediatric bipolar disorder using magnetoencephalography

Depression and Anxiety

Volumn 27, Issue 3, 2010, Pages 276-286

  Rich, Brendan A ^a   Holroyd, Tom ^b   Carver, Frederick W ^b   Onelio, Laura M ^b   Mendoza, Jennifer K ^b   Cornwell, Brian R ^b   Fox, Nathan A ^c   Pine, Daniel S ^b   Coppola, Richard ^b   Leibenluft, Ellen ^b  

^a CATHOLIC UNIVERSITY OF AMERICA   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Anterior cingulate cortex; Attention; Irritability; Neuroimaging; Parietal lobe; Theta

Indexed keywords

ANTIDEPRESSANT AGENT; ATYPICAL ANTIPSYCHOTIC AGENT; LITHIUM; MOOD STABILIZER; PSYCHOSTIMULANT AGENT;

ADOLESCENT; ANAMNESIS; ANXIETY DISORDER; ARTICLE; ATTENTION; ATTENTION DEFICIT DISORDER; BEHAVIOR; BIPOLAR DISORDER; BIPOLAR I DISORDER; BIPOLAR II DISORDER; CHILD PSYCHIATRY; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; EMOTION; FEMALE; FRUSTRATION; GENERALIZED ANXIETY DISORDER; HUMAN; MAGNETOENCEPHALOGRAPHY; MALE; NEGATIVE FEEDBACK; NERVE CELL; OSCILLATION; PARIETAL LOBE; PHOBIA; POSITIVE FEEDBACK; PRIORITY JOURNAL; REACTION TIME; SELF MONITORING; SELF REPORT; SEPARATION ANXIETY; STIMULUS; STIMULUS RESPONSE; THETA RHYTHM;

ADOLESCENT; AFFECT; BIPOLAR DISORDER; CHILD; EXPRESSED EMOTION; FEMALE; GYRUS CINGULI; HUMANS; MAGNETOENCEPHALOGRAPHY; MALE; NERVE NET; PARIETAL LOBE;

EID: 77649241825     PISSN: 10914269     EISSN: 15206394     Source Type: Journal    
DOI: 10.1002/da.20649     Document Type: Article

References (124)

1. Geller B, Williams M, Zimerman B, Frazier J, Beringer L, Warner KL. Prepubertal and early adolescent bipolarity differentiate from ADHD by manic symptoms, grandiose delusions, ultra-rapid or ultradian cycling. J Affect Disord 1998;51:81-91.
2. Carlson GA, Jensen PS, Findling RL, et al. Methodological issues and controversies in clinical trials with child and adolescent patients with bipolar disorder: report of a consensus conference. J Child Adolesc Psychopharmacol 2003;13:13-27.
3. Biederman J, Faraone SV, Wozniak J, Monuteaux MC. Parsing the association between bipolar, conduct, and substance use disorders: a familial risk analysis. Biol Psychiatry 2000;48: 1037-1044.
4. Perez-Edgar K, Fox N. A behavioral and electrophysiological study of children's selective attention under neutral and affective conditions. J Cogn Dev 2005;6:89-116.
5. Rich BA, Schmajuk M, Perez-Edgar KE, Pine DS, Fox NA, Leibenluft E. The impact of reward, punishment, and frustration on attention in pediatric bipolar disorder. Biol Psychiatry 2005;58:532-539.
6. Rich BA, Schmajuk M, Perez-Edgar KE, Fox NA, Pine DS, Leibenluft E. Different psychophysiological and behavioral responses elicited by frustration in pediatric bipolar disorder and severe mood dysregulation. Am J Psychiatry 2007;164: 309-317.
7. Hirata M, Koreeda S, Sakihara K, Kato A, Yoshimine T, Yorifuji S. Effects of the emotional connotations in words on the frontal areas-a spatially filtered MEG study. Neuroimage 2007;35:420-429.
8. Reite M, Teale P, Rojas DC. Magnetoencephalography: applications in psychiatry. Biol Psychiatry 1999;45:1553-1563.
9. Ioannides AA. Magnetoencephalography as a research tool in neuroscience: state of the art. Neuroscientist 2006;12:524-544.
10. Vrba J, Robinson SE. Signal processing in magnetoencephalography. Methods 2001;25:249-271.
11. Ishii R, Shinosaki K, Ukai S, et al. Medial prefrontal cortex generates frontal midline theta rhythm. Neuroreport 1999;10:675-679.
12. Taniguchi M, Kato A, Fujita N, et al. Movement-related desynchronization of the cerebral cortex studied with spatially filtered magnetoencephalography. Neuroimage 2000;12:298-306.
13. Schnitzler A, Gross J. Normal and pathological oscillatory communication in the brain. Nat Rev Neurosci 2005;6:285-296.
14. Aftanas LI, Varlamov AA, Pavlov SV, Makhnev VP, Reva NV. Affective picture processing: event-related synchronization within individually defined human theta band is modulated by valence dimension. Neurosci Lett 2001;303:115-118.
15. Adinoff B, Devous Sr MD, Best SM, George MS, Alexander D, Payne K. Limbic responsiveness to procaine in cocaine-addicted subjects. Am J Psychiatry 2001;58:390-398.
16. Aftanas LI, Golocheikine SA. Human anterior and frontal midline theta and lower alpha reflect emotionally positive state and internalized attention: high-resolution EEG investigation of meditation. Neurosci Lett 2001;310:57-60.
17. Knyazev GG. Motivation, emotion, and their inhibitory control mirrored in brain oscillations. Neurosci Biobehav Rev 2007;31: 377-395.
18. Aftanas LI, Reva NV, Varlamov AA, Pavlov SV, Makhnev VP. Analysis of evoked EEG synchronization and desynchronization in conditions of emotional activation in humans: temporal and topographic characteristics. Neurosci Behav Physiol 2004;34: 859-867.
19. Aftanas LI, Varlamov AA, Reva NV, Pavlov SV. Disruption of early event-related theta synchronization of human EEG in alexithymics viewing affective pictures. Neurosci Lett 2003;340: 57-60.
20. Salminen M, Ravaja N. Increased oscillatory theta activation evoked by violent digital game events. Neurosci Lett 2008;435: 69-72.
21. Nishitani N. Dynamics of cognitive processing in the human hippocampus by neuromagnetic and neurochemical assessments. Neuroimage 2003;20:561-571.
22. Sauseng P, Hoppe J, Klimesch W, Gerloff C, Hummel FC. Dissociation of sustained attention from central executive functions: local activity and interregional connectivity in the theta range. Eur J Neurosci 2007;25:587-593.
23. Doppelmayr M, Finkenzeller T, Sauseng P. Frontal midline theta in the pre-shot phase of rifle shooting: differences between experts and novices. Neuropsychologia 2008;46:1463-1467.
24. Luu P, Tucker DM, Derryberry D, Reed M, Poulsen C. Electrophysiological responses to errors and feedback in the process of action regulation. Psychol Sci 2003;14:47-53.
25. Luu P, Tucker DM, Makeig S. Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation. Clin Neurophysiol 2004;115:1821-1835.
26. Sammer G, Blecker C, Gebhardt H, et al. Relationship between regional hemodynamic activity and simultaneously recorded EEG-theta associated with mental arithmetic-induced workload. Hum Brain Mapp 2007;28:793-803.
27. Siegrist J, Menrath I, Stocker T, et al. Differential brain activation according to chronic social reward frustration. Neuroreport 2005;16:1899-1903.
28. Abler B, Walter H, Erk S. Neural correlates of frustration. Neuroreport 2005;16:669-672.
29. Wilke M, Kowatch RA, Delbello MP, Mills NP, Holland SK. Voxel-based morphometry in adolescents with bipolar disorder: first results. Psychiatry Res 2004;131:57-69.
30. Kaur S, Sassi RB, Axelson D, et al. Cingulate cortex anatomical abnormalities in children and adolescents with bipolar disorder. Am J Psychiatry 2005;162:1637-1643.
31. Chang K, Adleman NE, Dienes K, Simeonova DI, Menon V, Reiss A. Anomalous prefrontal-subcortical activation in familial pediatric bipolar disorder: a functional magnetic resonance imaging investigation. Arch Gen Psychiatry 2004;61:781-792.
32. Leibenluft E, Rich BA, Vinton DT, et al. Neural circuitry engaged during unsuccessful motor inhibition in pediatric bipolar disorder. Am J Psychiatry 2007;164:52-60.
33. Kaufman J, Birmaher B, Brent D, et al. 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 Psychiatry 1997;36:980-988.
34. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed.Washington, DC: American Psychiatric Press; 1994.
35. Geller B, Zimerman B, Williams M, et al. DSM-IV mania symptoms in a prepubertal and early adolescent bipolar disorder phenotype compared to attention-deficit hyperactive and normal controls. J Child Adolesc Psychopharmacol 2002;12:11-25.
36. Wechsler D. Wechsler Abbreviated Scale of Intelligence. San Antonio: The Psychological Corporation; 1999.
37. Poznanski EO, Grossman JA, Buchsbaum Y, Banegas M, Freeman L, Gibbons R. Preliminary studies of the reliability and validity of the Children's Depression Rating Scale. J Am Acad Child Psychiatry 1984;23:191-197.
38. Young RC, Biggs JT, Ziegler VE, Meyer DA. A rating scale for mania: reliability, validity and sensitivity. Br J Psychiatry 1978;133:429-435.
39. Shaffer D, Gould MS, Brasic J, et al. A Children's Global Assessment Scale (CGAS). Arch Gen Psychiatry 1983;40: 1228-1231.
40. Posner MI. Chronometric Explorations of the Mind. Hillsdale, NJ: Lawrence Erlbaum Associates; 1978.
41. McManis MH, Bradley MM, Berg WK, Cuthbert BN, Lang PJ. Emotional reactions in children: verbal, physiological, and behavioral responses to affective pictures. Psychophysiology 2001;38:222-231.
42. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996;29:162-173.
43. Drabycz S, Stockwell RG, Mitchell JR. Image texture characterization using the discrete orthonormal S-transform. J Digit Imaging 2008;22:696-708.
44. Aftanas LI, Varlamov AA, Reva NV, Pavlov SV. Disruption of early event-related theta synchronization of human EEG in alexithymics viewing affective pictures. Neurosci Lett 2003;340:57-60.
45. Salminen M, Ravaja N. Increased oscillatory theta activation evoked by violent digital game events. Neurosci Lett 2008;435:69-72.
46. Hanslmayr S, Pastotter B, Bauml KH, Gruber S, Wimber M, Klimesch W. The electrophysiological dynamics of interference during the Stroop task. J Cogn Neurosci 2008;20:215-225.
47. Sekihara K, Nagarajan SS, Poeppel D, Marantz A, Miyashita Y. Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique. IEEE Trans Biomed Eng 2001;48:760-771.
48. Cornwell BR, Baas JM, Johnson L, et al. Neural responses to auditory stimulus deviance under threat of electric shock revealed by spatially-filtered magnetoencephalography. Neuroimage 2007;37:282-289.
49. Luo Q, Holroyd T, Jones M, Hendler T, Blair J. Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG. Neuroimage 2007;34:839-847.
50. Aftanas LI, Varlamov AA, Pavlov SV, Makhnev VP, Reva NV. Time-dependent cortical asymmetries induced by emotional arousal: EEG analysis of event-related synchronization and desynchronization in individually defined frequency bands. Int J Psychophysiol 2002;44:67-82.
51. Pfurtscheller G, Lopes da Silva FH. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 1999;110:1842-1857.
52. Basar E, Schurmann M, Sakowitz O. The selectively distributed theta system: functions. Int J Psychophysiol 2001;39: 197-212.
53. Pizzagalli DA, Oakes TR, Davidson RJ. Coupling of theta activity and glucose metabolism in the human rostral anterior cingulate cortex: an EEG/PET study of normal and depressed subjects. Psychophysiology 2003;40:939-949.
54. Salvadore G, Cornwell BR, Colon-Rosario V, et al. Increased anterior cingulate cortical activity in response to fearful faces: a neurophysiological biomarker that predicts rapid antidepressant response to ketamine. Biol Psychiatry 2008;65:289-295.
55. Cornwell BR, Carver FW, Coppola R, Johnson L, Alvarez R, Grillon C. Evoked amygdala responses to negative faces revealed by adaptive MEG beamformers. Brain Res 2008;1244: 103-112.
56. Cornwell BR, Johnson LL, Holroyd T, Carver FW, Grillon C. Human hippocampal and parahippocampal theta during goaldirected spatial navigation predicts performance on a virtual Morris water maze. J Neurosci 2008;28:5983-5990.
57. Ogawa H, Wakita M, Hasegawa K, et al. Functional MRI detection of activation in the primary gustatory cortices in humans. Chem Senses 2005;30:583-592.
58. Lapalme E, Lina JM, Mattout J. Data-driven parceling and entropic inference in MEG. Neuroimage 2006;30:160-171.
59. Ossadtchi A, Baillet S, Mosher JC, Thyerlei D, Sutherling W, Leahy RM. Automated interictal spike detection and source localization in magnetoencephalography using independent components analysis and spatio-temporal clustering. Clin Neurophysiol 2004;115:508-522.
60. Nichols T, Hayasaka S. Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat Methods Med Res 2003;12:419-446.
61. Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002;15:870-878.
62. Kahkonen S, Yamashita H, Rytsala H, Suominen K, Ahveninen J, Isometsa E. Dysfunction in early auditory processing in major depressive disorder revealed by combined MEG and EEG. J Psychiatry Neurosci 2007;32:316-322.
63. Henson RN, Mattout J, Singh KD, Barnes GR, Hillebrand A, Friston K. Population-level inferences for distributed MEG source localization under multiple constraints: application to face-evoked fields. Neuroimage 2007;38:422-438.
64. Brunetti M, Della PS, Ferretti A, Del GC, Cianflone F, Belardinelli P, et al. A frontoparietal network for spatial attention reorienting in the auditory domain: a human fMRI/MEG study of functional and temporal dynamics. Cereb Cortex 2008;18: 1139-1147.
65. Onoda K, Okamoto Y, Shishida K, et al. Anticipation of affective images and event-related desynchronization (ERD) of alpha activity: an MEG study. Brain Res 2007;1151:134-141.
66. Statistical Package for Social Sciences for Windows, Version 16 [computer program]. Chicago: SPSS; 2007.
67. Adinoff B, Devous Jr MD, Best SM, George MS, Alexander D, Payne K. Limbic responsiveness to procaine in cocaine-addicted subjects. Am J Psychiatry 2001;158:390-398.
68. Luu P, Tucker DM, Derryberry D, Reed M, Poulsen C. Electrophysiological responses to errors and feedback in the process of action regulation. Psychol Sci 2003;14:47-53.
69. Taylor SF, Martis B, Fitzgerald KD, et al. Medial frontal cortex activity and loss-related responses to errors. J Neurosci 2006;26:4063-4070.
70. Holroyd CB, Nieuwenhuis S, Yeung N, et al. Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals. Nat Neurosci 2004;7:497-498.
71. Luu P, Pederson SM. The anterior cingulate cortex: regulating actions in context. In: Posner MI, editor. Cognitive Neuroscience of Attention. New York: Guilford Publication, Inc.; 2004.
72. Nieuwenhuis S, Ridderinkhof KR, Blom J, Band GP, Kok A. Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. Psychophysiology 2001;38:752-760.
73. Tzur G, Berger A. When things look wrong: theta activity in rule violation. Neuropsychologia 2007;45:3122-3126.
74. Desimone R, Duncan J. Neural mechanisms of selective visual attention. Annu Rev Neurosci 1995;18:193-222.
75. Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci 2001;24:167-202.
76. Posner MI, Petersen SE. The attention system of the human brain. Annu Rev Neurosci 1990;13:25-42.
77. Crick NR, Dodge KA. Social information-processing mechanisms in reactive and proactive aggression. Child Dev 1996;67:993-1002.
78. Wang F, Jackowski M, Kalmar JH, et al. Abnormal anterior cingulum integrity in bipolar disorder determined through diffusion tensor imaging. Br J Psychiatry 2008;193: 126-129.
79. Chiu S, Widjaja F, Bates ME, et al. Anterior cingulate volume in pediatric bipolar disorder and autism. J Affect Disord 2008;105:93-99.
80. Sassi RB, Brambilla P, Hatch JP, et al. Reduced left anterior cingulate volumes in untreated bipolar patients. Biol Psychiatry 2004;56:467-475.
81. Blumberg HP, Stern E, Martinez D, et al. Increased anterior cingulate and caudate activity in bipolar mania. Biol Psychiatry 2000;48:1045-1052.
82. Gruber SA. Decreased activation of the anterior cingulate in bipolar patients: an fMRI study. J Affect Disorders 2004;82:191-201.
83. Rubia K, Smith AB, Taylor E, Brammer M. Linear agecorrelated functional development of right inferior frontostriato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Hum Brain Mapp 2007;28:1163-1177.
84. Jonkman LM, Lansbergen M, Stauder JE. Developmental differences in behavioral and event-related brain responses associated with response preparation and inhibition in a go/nogo task. Psychophysiology 2003;40:752-761.
85. Johnstone SJ, Pleffer CB, Barry RJ, Clarke AR, Smith JL. Development of inhibitory processing during the go/nogo task. J Psychophysiol 2005;19:11-23.
86. Dimoska A, Johnstone SJ, Chiswick D, Barry RJ, Clarke AR. A developmental investigation of stop-signal inhibition: dissociating low- and higher-frequency activity in the eventrelated potential. J Psychophysiol 2007;21:109-126.
87. Bekker EM, Kenemans JL, Verbaten MN. Source analysis of the N2 in a cued Go/NoGo task. Brain Res Cogn Brain Res 2005;22:221-231.
88. Rubia K, Overmeyer S, Taylor E, et al. Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI. Neurosci Biobehav Rev 2000;24:13-19.
89. Booth JR, Burman DD, Meyer JR, et al. Neural development of selective attention and response inhibition. Neuroimage 2003;20:737-751.
90. Frazier JA, Breeze JL, Makris N, et al. Cortical gray matter differences identified by structural magnetic resonance imaging in pediatric bipolar disorder. Bipolar Disord 2005;7: 555-569.
91. Adler CM, Delbello MP, Mills NP, Schmithorst V, Holland S, Strakowski SM. Comorbid ADHD is associated with altered patterns of neuronal activation in adolescents with bipolar disorder performing a simple attention task. Bipolar Disord 2005;7:577-588.
92. Posner MI, Sheese BE, Odludas Y, Tang Y. Analyzing and shaping human attentional networks. Neural Netw 2006;19:1422-1429.
93. Satpute AB, Lieberman MD. Integrating automatic and controlled processes into neurocognitive models of social cognition. Brain Res 2006;1079:86-97.
94. Lieberman MD, Jarcho JM, Satpute AB. Evidence-based and intuition-based self-knowledge: an FMRI study. J Pers Soc Psychol 2004;87:421-435.
95. Labudda K, Woermann FG, Mertens M, Pohlmann-Eden B, Markowitsch HJ, Brand M. Neural correlates of decision making with explicit information about probabilities and incentives in elderly healthy subjects. Exp Brain Res 2008;187:641-650.
96. Fehr T, Kissler J, Wienbruch C, et al. Source distribution of neuromagnetic slow-wave activity in schizophrenic patients-effects of activation. Schizophr Res 2003;63:63-71.
97. Caligiuri MP, Brown GG, Meloy MJ, et al. An fMRI study of affective state and medication on cortical and subcortical brain regions during motor performance in bipolar disorder. Psychiatry Res 2003;123:171-182.
98. Nelson EE, Vinton DT, Berghorst L, et al. Brain systems underlying response flexibility in healthy and bipolar adolescents: an event-related fMRI study. Bipolar Disord 2007;9: 810-819.
99. Blumberg HP, Donegan NH, Sanislow CA, et al. Preliminary evidence for medication effects on functional abnormalities in the amygdala and anterior cingulate in bipolar disorder. Psychopharmacology (Berl) 2005;183:308-313.
100. Smith ME, Gevins A, McEvoy LK, Meador KJ, Ray PG, Gilliam F. Distinct cognitive neurophysiologic profiles for lamotrigine and topiramate. Epilepsia 2006;47:695-703.
101. Rohayem J, Bayle JF, Richa S. Predictors of prophylactic response to lithium. Encephale 2008;34:394-399.
102. Suslov NI, Fedorov AA, Pershina OV, Borodin YI, Rachkovskaya LN. Effect of Noolit, a novel lithium preparation, on electrophysiological activity of rat cerebral cortex. Bull Exp Biol Med 2004;137:155-158.
103. Schulz C, Mavrogiorgou P, Schroter A, Hegerl U, Juckel G. Lithium-induced EEG changes in patients with affective disorders. Neuropsychobiology 2000;42:33-37.
104. Gholmieh GI, Courellis SH, Chen LS. Screening for the effects of antiepileptic drugs on short term plasticity using a time efficient bioassay. Conf Proc IEEE Eng Med Biol Soc 2007;2007:2247-2252.
105. Clemens B, Menes A, Piros P, et al. Quantitative EEG effects of carbamazepine, oxcarbazepine, valproate, lamotrigine, and possible clinical relevance of the findings. Epilepsy Res 2006;70:190-199.
106. Clemens B. Valproate decreases EEG synchronization in a usedependent manner in idiopathic generalized epilepsy. Seizure 2008;17:224-233.
107. Iosifescu DV, Greenwald S, Devlin P, et al. Frontal EEG predictors of treatment outcome in major depressive disorder. Eur Neuropsychopharmacol 2009;19:772-777.
108. Dumont GJ, de Visser SJ, Cohen AF, van Gerven JM. Biomarkers for the effects of selective serotonin reuptake inhibitors (SSRIs) in healthy subjects. Br J Clin Pharmacol 2005;59:495-510.
109. Holmes AJ, Pizzagalli DA. Spatiotemporal dynamics of error processing dysfunctions in major depressive disorder. Arch Gen Psychiatry 2008;65:179-188.
110. Tucker DM, Luu P, Frishkoff G, Quiring J, Poulsen C. Frontolimbic response to negative feedback in clinical depression. J Abnorm Psychol 2003;112:667-678.
111. Chiu PH, Deldin PJ. Neural evidence for enhanced error detection in major depressive disorder. Am J Psychiatry 2007;164:608-616.
112. Holmes AJ, Pizzagalli DA. Response conflict and frontocingulate dysfunction in unmedicated participants with major depression. Neuropsychologia 2008;46:2904-2913.
113. Santesso DL, Steele KT, Bogdan R, et al. Enhanced negative feedback responses in remitted depression. Neuroreport 2008;19:1045-1048.
114. Santesso DL, Dillon DG, Birk JL, et al. Individual differences in reinforcement learning: behavioral, electrophysiological, and neuroimaging correlates. Neuroimage 2008;42:807-816.
115. Chiu PH, Holmes AJ, Pizzagalli DA. Dissociable recruitment of rostral anterior cingulate and inferior frontal cortex in emotional response inhibition. Neuroimage 2008;42:988-997.
116. Callicott JH, Weinberger DR. Neuropsychiatric dynamics: the study of mental illness using functional magnetic resonance imaging. Eur J Radiol 2000;30:95-104.
117. Callicott JH, Mattay VS, Verchinski BA, Marenco S, Egan MF, Weinberger DR. Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. Am J Psychiatry 2003;160:2209-2215.
118. Wilkinson D, Halligan P. The relevance of behavioural measures for functional-imaging studies of cognition. Nat Rev Neurosci 2004;5:67-73.
119. Blumberg HP, Fredericks C, Wang F, et al. Preliminary evidence for persistent abnormalities in amygdala volumes in adolescents and young adults with bipolar disorder. Bipolar Disord 2005;7:570-576.
120. Chang K, Karchemskiy A, Barnea-Goraly N, Garrett A, Simeonova DI, Reiss A. Reduced amygdalar gray matter volume in familial pediatric bipolar disorder. J Am Acad Child Adolesc Psychiatry 2005;44:565-573.
121. Sanches M, Sassi RB, Axelson D, et al. Subgenual prefrontal cortex of child and adolescent bipolar patients: a morphometric magnetic resonance imaging study. Psychiatry Res 2005;138:43-49.
122. Chen BK, Sassi R, Axelson D, et al. Cross-sectional study of abnormal amygdala development in adolescents and young adults with bipolar disorder. Biol Psychiatr 2004;56: 399-405.
123. Delbello MP, Zimmerman ME, Mills NP, Getz GE, Strakowski SM. Magnetic resonance imaging analysis of amygdala and other subcortical brain regions in adolescents with bipolar disorder. Bipolar Disord 2004;6:43-52.
124. Frazier JA, Chiu S, Breeze JL, et al. Structural brain magnetic resonance imaging of limbic and thalamic volumes in pediatric bipolar disorder. Am J Psychiatry 2005;162:1256-1265.