Hippocampal volume development in healthy siblings of childhood-onset schizophrenia patients

American Journal of Psychiatry

Volumn 168, Issue 4, 2011, Pages 427-435

  Mattai, Anand ^a,b   Hosanagar, Avinash ^a,b   Weisinger, Brian ^a,b   Greenstein, Deanna ^a,b   Stidd, Reva ^a,b   Clasen, Liv ^a,b   Lalonde, Francois ^a,b   Rapoport, Judith ^a,b   Gogtay, Nitin ^a,b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; AGE; ARTICLE; BRAIN SIZE; CHILDHOOD ONSET SCHIZOPHRENIA; COMPUTER PROGRAM; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SCHIZOPHRENIA;

ADOLESCENT; ADULT; AGE FACTORS; AGE OF ONSET; CASE-CONTROL STUDIES; CHILD; FEMALE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; ORGAN SIZE; PSYCHIATRIC STATUS RATING SCALES; SCHIZOPHRENIA; SIBLINGS; YOUNG ADULT;

EID: 79955142750     PISSN: 0002953X     EISSN: 15357228     Source Type: Journal    
DOI: 10.1176/appi.ajp.2010.10050681     Document Type: Article

References (87)

1. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J: Regional dissociations within the hippocampus: memory and anxiety. Neurosci Biobehav Rev 2004;28:273-283 (Pubitemid 38844376)
2. Vargha-Khadem F, Gadian DG, Watkins KE, Connelly A, Van Paesschen W, Mishkin M: Differential effects of early hippocampal pathology on episodic and semantic memory. Science 1997;277:376-380 (Pubitemid 27450711)
3. Squire LR, Alvarez P: Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol 1995;5:169-177
4. Tulving E, Markowitsch HJ, Craik FE, Habib R, Houle S: Novelty and familiarity activations in PET studies of memory encoding and retrieval. Cereb Cortex 1996;6:71-79
5. Grunwald T, Kurthen M: Novelty detection and encoding for declarative memory within the human hippocampus. Clin EEG Neurosci 2006;37:309-314 (Pubitemid 44625544)
6. Henke K, Weber B, Kneifel S, Wieser HG, Buck A: Human hippocampus associates information in memory. Proc Natl Acad Sci USA 1999;96:5884-5889 (Pubitemid 29234713)
7. Honea R, Crow TJ, Passingham D, Mackay CE: Regional deficits in brain volume in schizophrenia: a metaanalysis of voxelbased morphometry studies. Am J Psychiatry 2005;162:2233-2245 (Pubitemid 41740200)
8. Steen RG, Mull C, McClure R, Hamer RM, Lieberman JA: Brain volume in firstepisode schizophrenia: systematic review and metaanalysis of magnetic resonance imaging studies. Br J Psychiatry 2006;188:510-518 (Pubitemid 43844097)
9. Vita A, De Peri L, Silenzi C, Dieci M: Brain morphology in firstepisode schizophrenia: a metaanalysis of quantitative magnetic resonance imaging studies. Schizophr Res 2006;82:75-88 (Pubitemid 43202650)
10. Harrison PJ: The neuropathology of schizophrenia: a critical review of the data and their interpretation. Brain 1999;122(pt 4):593-624 (Pubitemid 29158770)
11. Harrison PJ: The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology (Berl) 2004;174:151-162 (Pubitemid 38925100)
12. Benes FM, Sorensen I, Bird ED: Reduced neuronal size in posterior hippocampus of schizophrenic patients. Schizophr Bull 1991;17:597-608
13. Giedd JN, Jeffries NO, Blumenthal J, Castellanos FX, Vaituzis AC, Fernandez T, Hamburger SD, Liu H, Nelson J, Bedwell J, Tran L, Lenane M, Nicolson R, Rapoport JL: Childhoodonset schizophrenia: progressive brain changes during adolescence. Biol Psychiatry 1999;46:892-898 (Pubitemid 29452980)
14. Greenstein D, Lerch J, Shaw P, Clasen L, Giedd J, Gochman P, Rapoport J, Gogtay N: Childhood onset schizophrenia: cortical brain abnormalities as young adults. J Child Psychol Psychiatry 2006;47:1003-1012 (Pubitemid 44642429)
15. Gogtay N, Nugent TF 3rd, Herman DH, Ordonez A, Greenstein D, Hayashi KM, Clasen L, Toga AW, Giedd JN, Rapoport JL, Thompson PM: Dynamic mapping of normal human hippocampal development. Hippocampus 2006;16:664-672 (Pubitemid 44649480)
16. Seidman LJ, Faraone SV, Goldstein JM, Kremen WS, Horton NJ, Makris N, Toomey R, Kennedy D, Caviness VS, Tsuang MT: Left hippocampal volume as a vulnerability indicator for schizophrenia: a magnetic resonance imaging morphometric study of nonpsychotic firstdegree relatives. Arch Gen Psychiatry 2002;5:839-849 (Pubitemid 35001150)
17. Nelson MD, Saykin AJ, Flashman LA, Riordan HJ: Hippocampal volume reduction in schizophrenia as assessed by magnetic resonance imaging: a metaanalytic study. Arch Gen Psychiatry 1998;55:433-440 (Pubitemid 28237277)
18. Keshavan MS, Prasad KM, Pearlson G: Are brain structural abnormalities useful as endophenotypes in schizophrenia? Int Rev Psychiatry 2007;19:399-408 (Pubitemid 47206982)
19. Wickham H, Murray RM: Can biological markers identify endophenotypes predisposing to schizophrenia? Int Rev Psychiatry 1997;9:355-364 (Pubitemid 27499492)
20. Ho BC, Magnotta V: Hippocampal volume deficits and shape deformities in young biological relatives of schizophrenia probands. Neuroimage 2009;49:3385-3393
21. van Haren NE, Picchioni MM, McDonald C, Marshall N, Davis N, Ribchester T, Hulshoff Pol HE, Sharma T, Sham P, Kahn RS, Murray R: A controlled study of brain structure in monozygotic twins concordant and discordant for schizophrenia. Biol Psychiatry 2004;56:454-461 (Pubitemid 39195326)
22. Tepest R, Wang L, Miller MI, Falkai P, Csernansky JG: Hippocampal deformities in the unaffected siblings of schizophrenia subjects. Biol Psychiatry 2003;54:1234-1240 (Pubitemid 37464869)
23. van Erp TG, Saleh PA, Rosso IM, Huttunen M, Lonnqvist J, Pirkola T, Salonen O, Valanne L, Poutanen VP, Standertskjöld-Nordenstam CG, Cannon TD: Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings, and healthy unrelated volunteers. Am J Psychiatry 2002;159:1514-1520 (Pubitemid 35006731)
24. Honea RA, Meyer-Lindenberg A, Hobbs KB, Pezawas L, Mattay VS, Egan MF, Verchinski B, Passingham RE, Weinberger DR, Callicott JH: Is gray matter volume an intermediate phenotype for schizophrenia?: a voxelbased morphometry study of patients with schizophrenia and their healthy siblings. Biol Psychiatry 2008;63:465-474 (Pubitemid 351227356)
25. McDonald C, Marshall N, Sham PC, Bullmore ET, Schulze K, Chapple B, Bramon E, Filbey F, Quraishi S, Walshe M, Murray RM: Regional brain morphometry in patients with schizophrenia or bipolar disorder and their unaffected relatives. Am J Psychiatry 2006;163:478-487 (Pubitemid 44469391)
26. Goldman AL, Pezawas L, Mattay VS, Fischl B, Verchinski BA, Zoltick B, Weinberger DR, Meyer-Lindenberg A: Heritability of brain morphology related to schizophrenia: a largescale automated magnetic resonance imaging segmentation study. Biol Psychiatry 2008;63:475-483 (Pubitemid 351227357)
27. Staal WG, Hulshoff Pol HE, Schnack HG, Hoogendoorn ML, Jellema K, Kahn RS: Structural brain abnormalities in patients with schizophrenia and their healthy siblings. Am J Psychiatry 2000;157:416-421 (Pubitemid 30145928)
28. Narr KL, van Erp TGM, Cannon TD, Woods RP, Thompson PM, Jang S, Blanton R, Poutanen VP, Huttunen M, Lönnqvist J, Standerksjöld-Nordenstam CG, Kaprio J, Mazziotta JC, Toga AW: A twin study of genetic contributions to hippocampal morphology in schizophrenia. Neurobiol Dis 2002;11:83-95 (Pubitemid 35435676)
29. Baaré WF, van Oel CJ, Hulshoff Pol HE, Schnack HG, Durston S, Sitskoorn MM, Kahn RS: Volumes of brain structures in twins discordant for schizophrenia. Arch Gen Psychiatry 2001;58:33-40 (Pubitemid 32057763)
30. Buehlmann E, Berger GE, Aston J, Gschwandtner U, Pflueger MO, Borgwardt SJ, Radue EW, Riecher-Rössler A: Hippocampus abnormalities in at risk mental states for psychosis? a crosssectional high resolution region of interest magnetic resonance imaging study. J Psychiatr Res 2010;44:447-453
31. Velakoulis D, Wood SJ, Wong MTH, McGorry PD, Yung A, Phillips L, Smith D, Brewer W, Proffitt T, Desmond P, Pantelis C: Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, firstepisode psychosis, and ultrahighrisk individuals. Arch Gen Psychiatry 2006;63:139-149 (Pubitemid 43213875)
32. Velakoulis D, Pantelis C, McGorry PD, Dudgeon P, Brewer W, Cook M, Desmond P, Bridle N, Tierney P, Murrie V, Singh B, Copolov D: Hippocampal volume in firstepisode psychoses and chronic schizophrenia: a highresolution magnetic resonance imaging study. Arch Gen Psychiatry 1999;56:133-141
33. Phillips LJ, Velakoulis D, Pantelis C, Wood S, Yuen HP, Yung AR, Desmond P, Brewer W, McGorry PD: Nonreduction in hippocampal volume is associated with higher risk of psychosis. Schizophr Res 2002;58:145-158 (Pubitemid 35284506)
34. Witthaus H, Kaufmann C, Bohner G, Ozgurdal S, Gudlowski Y, Gallinat J, Ruhrmann S, Brüne M, Heinz A, Klingebiel R, Juckel G: Gray matter abnormalities in subjects at ultrahigh risk for schizophrenia and firstepisode schizophrenic patients compared to healthy controls. Psychiatry Res 2009;173:163-169
35. Witthaus H, Mendes U, Brune M, Ozgurdal S, Bohner G, Gudlowski Y, Kalus P, Andreasen N, Heinz A, Klingebiel R, Juckel G: Hippocampal subdivision and amygdalar volumes in patients in an atrisk mental state for schizophrenia. J Psychiatry Neurosci 2010;35:33-40
36. Sismanlar SG, Anik Y, Coskun A, Agaoglu B, Karakaya I, Yavuz CI: The volumetric differences of the frontotemporal region in young offspring of schizophrenic patients. Eur Child Adolesc Psychiatry 2009;19:151-157
37. Nicolson R, Rapoport JL: Childhoodonset schizophrenia: rare but worth studying. Biol Psychiatry 1999;46:1418-1428
38. Gogtay N, Sporn A, Clasen LS, Nugent TF 3rd, Greenstein D, Nicolson R, Giedd JN, Lenane M, Gochman P, Evans A, Rapoport JL: Comparison of progressive cortical gray matter loss in childhoodonset schizophrenia with that in childhoodonset atypical psychoses. Arch Gen Psychiatry 2004;61:17-22 (Pubitemid 38044637)
39. Sporn AL, Greenstein DK, Gogtay N, Jeffries NO, Lenane M, Gochman P, Clasen LS, Blumenthal J, Giedd JN, Rapoport JL: Progressive brain volume loss during adolescence in childhoodonset schizophrenia. Am J Psychiatry 2003;160:2181-2189 (Pubitemid 39619611)
40. Gogtay N: Cortical brain development in schizophrenia: insights from neuroimaging studies in childhoodonset schizophrenia. Schizophr Bull 2008;34:30-36 (Pubitemid 350262284)
41. Arango C, Moreno C, Martinez S, Parellada M, Desco M, Moreno D, Fraguas D, Gogtay N, James A, Rapoport J: Longitudinal brain changes in earlyonset psychosis. Schizophr Bull 2008;34:341-353 (Pubitemid 351323337)
42. Nugent TF 3rd, Herman DH, Ordonez A, Greenstein D, Hayashi KM, Lenane M, Clasen L, Jung D, Toga AW, Giedd JN, Rapoport JL, Thompson PM, Gogtay N: Dynamic mapping of hippocampal development in childhood onset schizophrenia. Schizophr Res 2007;90:62-70 (Pubitemid 46177567)
43. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM: Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002;33:341-355 (Pubitemid 34162530)
44. McKenna K, Gordon CT, Lenane M, Kaysen D, Fahey K, Rapoport JL: Looking for childhoodonset schizophrenia: the first 71 cases screened. J Am Acad Child Adolesc Psychiatry 1994;33:636-644 (Pubitemid 24167020)
45. Endicott J, Spitzer RL: Schedule for Affective Disorders and Schizophrenia (SADS). Acta Psychiatr Belg 1987;87:361-516
46. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N: Schedule for Affective Disorders and Schizophrenia for SchoolAge Children-Present and Lifetime Version (KSADSPL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 1997;36:980-988 (Pubitemid 27272932)
47. Stangl D, Pfohl B, Zimmerman M, Bowers W, Corenthal C: A structured interview for the DSMIII personality disorders: a preliminary report. Arch Gen Psychiatry 1985;42:591-596 (Pubitemid 15058336)
48. Asarnow RF, Nuechterlein KH, Fogelson D, Subotnik KL, Payne DA, Russell AT, Asamen J, Kuppinger H, Kendler KS: Schizophrenia and schizophreniaspectrum personality disorders in the firstdegree relatives of children with schizophrenia: the UCLA Family Study. Arch Gen Psychiatry 2001;58:581-588 (Pubitemid 32523739)
49. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL: Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 1999;2:861-863 (Pubitemid 30602596)
50. Castellanos FX, Giedd JN, Berquin PC, Walter JM, Sharp W, Tran T, Vaituzis AC, Blumenthal JD, Nelson J, Bastain TM, Zijdenbos A, Evans AC, Rapoport JL: Quantitative brain magnetic resonance imaging in girls with attentiondeficit/hyperactivity disorder. Arch Gen Psychiatry 2001;58:289-295 (Pubitemid 32209683)
51. Fischl B, Salat DH, van der Kouwe AJ, Makris N, Segonne F, Quinn BT, Dale AM: Sequenceindependent segmentation of magnetic resonance images. Neuroimage 2004;23(suppl 1): S69-S84 (Pubitemid 39429376)
52. Ségonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B: A hybrid approach to the skull stripping problem in MRI. Neuroimage 2004;22:1060-1075 (Pubitemid 38829195)
53. Fischl B, Liu A, Dale AM: Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 2001;20:70-80 (Pubitemid 32293421)
54. Segonne F, Pacheco J, Fischl B: Geometrically accurate topologycorrection of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 2007;26:518-529 (Pubitemid 46527332)
55. Han X, Jovicich J, Salat D, van der Kouwe A, Quinn B, Czanner S, Busa E, Pacheco J, Albert M, Killiany R, Maguire P, Rosas D, Makris N, Dale A, Dickerson B, Fischl B: Reliability of MRIderived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. Neuroimage 2006;32:180-194
56. Weinberger DR: Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 1987;44:660-669 (Pubitemid 17099795)
57. Rapoport JL, Addington AM, Frangou S, Psych M: The neurodevelopmental model of schizophrenia: update 2005. Mol Psychiatry 2005;10:434-449 (Pubitemid 40646432)
58. Tseng KY, Lewis BL, Hashimoto T, Sesack SR, Kloc M, Lewis DA, O'Donnell P: A neonatal ventral hippocampal lesion causes functional deficits in adult prefrontal cortical interneurons. J Neurosci 2008;28:12691-12699
59. Lipska BK, Jaskiw GE, Weinberger DR: Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia. Neuropsychopharmacology 1993;9:67-75 (Pubitemid 23242602)
60. Velakoulis D, Wood SJ, Wong MT, McGorry PD, Yung A, Phillips L, Smith D, Brewer W, Proffitt T, Desmond P, Pantelis C: Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, firstepisode psychosis, and ultrahighrisk individuals. Arch Gen Psychiatry 2006;63:139-149 (Pubitemid 43213875)
61. Lieberman J, Chakos M, Wu H, Alvir J, Hoffman E, Robinson D, Bilder R: Longitudinal study of brain morphology in first episode schizophrenia. Biol Psychiatry 2001;49:487-499 (Pubitemid 32226407)
62. Chakos MH, Schobel SA, Gu H, Gerig G, Bradford D, Charles C, Lieberman JA: Duration of illness and treatment effects on hippocampal volume in male patients with schizophrenia. Br J Psychiatry 2005;186:26-31 (Pubitemid 40070540)
63. Ebdrup BH, Glenthoj B, Rasmussen H, Aggernaes B, Langkilde AR, Paulson OB, Lublin H, Skimminge A, Baaré W: Hippocampal and caudate volume reductions in antipsychoticnaive firstepisode schizophrenia. J Psychiatry Neurosci 2010;35:95-104
64. Mattai A, Chavez A, Greenstein D, Clasen L, Bakalar J, Stidd R, Rapoport J, Gogtay N: Effects of clozapine and olanzapine on cortical thickness in childhoodonset schizophrenia. Schizophr Res 2010;116:44-48
65. Arnold SE: Cellular and molecular neuropathology of the parahippocampal region in schizophrenia. Ann NY Acad Sci 2000;911:275-292 (Pubitemid 30462088)
66. Harrison PJ: The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology 2004;174:151-162 (Pubitemid 38925100)
67. Brown AS, Susser ES: In utero infection and adult schizophrenia. M ent Retard Dev Disabil Res Rev 2002;8:51-57 (Pubitemid 34754494)
68. Cannon M, Jones PB, Murray RM: Obstetric complications and schizophrenia: historical and metaanalytic review. Am J Psychiatry 2002;159:1080-1092 (Pubitemid 34743246)
69. Brown AS, Derkits EJ: Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry 2010;167:261-280
70. Mittal VA, Ellman LM, Cannon TD: Geneenvironment interaction and covariation in schizophrenia: the role of obstetric complications. Schizophr Bull 2008;34:1083-1094
71. DeLisi LE, Dauphinais ID, Gershon ES: Perinatal complications and reduced size of brain limbic structures in familial schizophrenia. Schizophr Bull 1988;14:185-191
72. Elsharkawy AE, Pannek H, Woermann FG, Gyimesi C, Hartmann S, Aengenendt J, Ogutu T, Hoppe M, Schulz R, Pietilä TA, Ebner A: Apical temporal lobe resection: "tailored" hippocampussparing resection based on presurgical evaluation data. Acta Neurochir (Epub ahead of print, July 17, 2010)
73. Rees S, Inder T: Fetal and neonatal origins of altered brain development. Early Hum Dev 2005;81:753-761 (Pubitemid 41253520)
74. Boksa P: Animal models of obstetric complications in relation to schizophrenia. Brain Res Brain Res Rev 2004;45:1-17 (Pubitemid 38520012)
75. McNeil TF, Cantor-Graae E, Weinberger DR: Relationship of obstetric complications and differences in size of brain structures in monozygotic twin pairs discordant for schizophrenia. Am J Psychiatry 2000;157:203-212 (Pubitemid 30080899)
76. van Erp TG, Saleh PA, Huttunen M, Lonnqvist J, Kaprio J, Salonen O, Valanne L, Poutanen VP, Standertskjöld-Nordenstam CG, Cannon TD: Hippocampal volumes in schizophrenic twins. Arch Gen Psychiatry 2004;61:346-353 (Pubitemid 38451543)
77. Nicolson R, Malaspina D, Giedd JN, Hamburger S, Lenane M, Bedwell J, Fernandez T, Berman A, Susser E, Rapoport JL: Obstetrical complications and childhoodonset schizophrenia. Am J Psychiatry 1999;156:1650-1652
78. McEwen BS: Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann N y Acad Sci 2001;933:265-277 (Pubitemid 32390122)
79. Bremner JD: Stress and brain atrophy. CNS Neurol Disord Drug Targets 2006;5:503-512 (Pubitemid 44523868)
80. Czyrak A, Mackowiak M, Chocyk A, Fijal K, Wedzony K: Role of glucocorticoids in the regulation of dopaminergic neurotransmission. Pol J Pharmacol 2003;55:667-674 (Pubitemid 37540864)
81. Moghaddam B: Stress activation of glutamate neurotransmission in the prefrontal cortex: implications for dopamineassociated psychiatric disorders. Biol Psychiatry 2002;51:775-787 (Pubitemid 34451064)
82. Suvisaari JM, Haukka JK, Tanskanen AJ, Lonnqvist JK: Decline in the incidence of schizophrenia in Finnish cohorts born from 1954 to 965. Arch Gen Psychiatry 1999;56:733-740 (Pubitemid 29357735)
83. Warner R: Time trends in schizophrenia: changes in obstetric risk factors with industrialization. Schizophr Bull 1995;21:483-500
84. DeCarolis NA, Eisch AJ: Hippocampal neurogenesis as a target for the treatment of mental illness: a critical evaluation. Neuropharmacology 2010;58:884-893
85. Reif A, Schmitt A, Fritzen S, Lesch KP: Neurogenesis and schizophrenia: dividing neurons in a divided mind? Eur Arch Psychiatry Clin Neurosci 2007;257:290-299 (Pubitemid 47301407)
86. Berchtold NC, Castello N, Cotman CW: Exercise and timedependent benefits to learning and memory. Neuroscience 2010;167:588-597
87. Pajonk FG, Wobrock T, Gruber O, Scherk H, Berner D, Kaizl I, Kierer A, Müller S, Oest M, Meyer T, Backens M, Schneider-Axmann T, Thornton AE, Honer WG, Falkai P: Hippocampal plasticity in response to exercise in schizophrenia. Arch Gen Psychiatry 2010;67:133-143