Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-02T20:37:40.868Z Has data issue: false hasContentIssue false
  • English
  • Français

Amygdala–hippocampal shape and cortical thickness abnormalities in first-episode schizophrenia and mania

Published online by Cambridge University Press:  28 November 2012

A. Qiu ,
S. C. Gan ,
Y. Wang  and
K. Sim
A. Qiu*
Affiliation:
Department of Bioengineering, National University of Singapore, Singapore Clinical Imaging Research Center, National University of Singapore, Singapore Singapore Institute for Clinical Sciences, the Agency for Science, Technology and Research, Singapore
S. C. Gan
Affiliation:
Department of Bioengineering, National University of Singapore, Singapore
Y. Wang
Affiliation:
Department of Bioengineering, National University of Singapore, Singapore
K. Sim
Affiliation:
Research Division, Institute of Mental Health, Singapore Department of General Psychiatry, Institute of Mental Health, Singapore
*
*Address for correspondence: A/Professor A. Qiu, Department of Bioengineering, National University of Singapore, 9 Engineering Drive 1, Block EA #03-12, Singapore117576. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Abnormalities in cortical thickness and subcortical structures have been studied in schizophrenia but little is known about corresponding changes in mania and brain structural differences between these two psychiatric conditions, especially early in the stage of the illness. In this study we aimed to compare cortical thickness and shape of the amygdala–hippocampal complex in first-episode schizophrenia (FES) and mania (FEM).

Method

Structural magnetic resonance imaging (MRI) was performed on 28 FES patients, 28 FEM patients and 28 healthy control subjects who were matched for age, gender and handedness.

Results

Overall, the shape of the amygdala was deformed in both patient groups, relative to controls. Compared to FEM patients, FES patients had significant inward shape deformation in the left hippocampal tail, right hippocampal body and a small region in the right amygdala. Cortical thinning was more widespread in FES patients, with significant differences found in the temporal brain regions when compared with FEM and controls.

Conclusions

Significant differences were observed between the two groups of patients with FES and FEM in terms of the hippocampal shape and cortical thickness in the temporal region, highlighting that distinguishable brain structural changes are present early in the course of schizophrenia and mania.

Keywords

Cortical thicknessfirst-episode schizophreniamaniastructural magnetic resonance imagingsubcortical shape
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 7 , July 2013 , pp. 1353 - 1363
Copyright
Copyright © Cambridge University Press 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adolphs, R, Tranel, D, Damasio, H, Damasio, AR (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372, 669–672.CrossRefGoogle Scholar
Adriano, F, Caltagirone, C, Spalletta, G (2012). Hippocampal volume reduction in first-episode and chronic schizophrenia: a review and meta-analysis. The Neuroscientist 18, 180–200.CrossRefGoogle ScholarPubMed
Altshuler, LL, Ventura, J, Van Gorp, WG, Green, MF, Theberge, DC, Mintz, J (2004). Neurocognitive function in clinically stable men with bipolar I disorder or schizophrenia and normal control subjects. Biological Psychiatry 56, 560–569.CrossRefGoogle ScholarPubMed
Atmaca, M, Ozdemir, H, Cetinkaya, S, Parmaksiz, S, Belli, H, Kursad Poyraz, A, Tezcan, E, Ogur, E (2007). Cingulate gyrus volumetry in drug free bipolar patients and patients treated with valproate or valproate and quetiapine. Journal of Psychiatric Research 41, 821–827.CrossRefGoogle ScholarPubMed
Bechara, A, Damasio, H, Damasio, AR (2000). Emotion, decision making and the orbitofrontal cortex. Cerebral Cortex 10, 295–307.CrossRefGoogle ScholarPubMed
Bechdolf, A, Wood, SJ, Nelson, B, Velakoulis, D, Yucel, M, Takahashi, T, Yung, AR, Berk, M, Wong, MT, Pantelis, C, McGorry, PD (2012). Amygdala and insula volumes prior to illness onset in bipolar disorder: a magnetic resonance imaging study. Psychiatry Research 201, 34–39.CrossRefGoogle ScholarPubMed
Bodnar, M, Malla, AK, Czechowska, Y, Benoit, A, Fathalli, F, Joober, R, Pruessner, M, Pruessner, J, Lepage, M (2010). Neural markers of remission in first-episode schizophrenia: a volumetric neuroimaging study of the hippocampus and amygdala. Schizophrenia Research 122, 72–80.CrossRefGoogle ScholarPubMed
Cascella, NG, Fieldstone, SC, Rao, VA, Pearlson, GD, Sawa, A, Schretlen, DJ (2010). Gray-matter abnormalities in deficit schizophrenia. Schizophrenia Research 120, 63–70.CrossRefGoogle ScholarPubMed
Chan, D, Anderson, V, Pijnenburg, Y, Whitwell, J, Barnes, J, Scahill, R, Stevens, JM, Barkhof, F, Scheltens, P, Rossor, MN, Fox, NC (2009). The clinical profile of right temporal lobe atrophy. Brain 132, 1287–1298.CrossRefGoogle ScholarPubMed
Chen, G, Zeng, WZ, Yuan, PX, Huang, LD, Jiang, YM, Zhao, ZH, Manji, HK (1999). The mood-stabilizing agents lithium and valproate robustly increase the levels of the neuroprotective protein bcl-2 in the CNS. Journal of Neurochemistry 72, 879–882.CrossRefGoogle ScholarPubMed
Chung, MK, Robbins, SM, Dalton, KM, Davidson, RJ, Alexander, AL, Evans, AC (2005). Cortical thickness analysis in autism with heat kernel smoothing. NeuroImage 25, 1256–1265.CrossRefGoogle ScholarPubMed
Chung, MK, Worsley, KJ, Nacewicz, BM, Dalton, KM, Davidson, RJ (2010). General multivariate linear modeling of surface shapes using SurfStat. NeuroImage 53, 491–505.CrossRefGoogle ScholarPubMed
Csernansky, JG, Joshi, S, Wang, L, Haller, JW, Gado, M, Miller, JP, Grenander, U, Miller, MI (1998). Hippocampal morphometry in schizophrenia by high dimensional brain mapping. Proceedings of the National Academy of Sciences USA 95, 11406–11411.CrossRefGoogle ScholarPubMed
Depue, RA, Collins, PF (1999). Neurobiology of the structure of personality: dopamine, facilitation of incentive motivation, and extraversion. Behavioral and Brain Sciences 22, 491–517.CrossRefGoogle ScholarPubMed
Eichenbaum, H (2000). A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience 1, 41–50.CrossRefGoogle ScholarPubMed
Einat, H, Yuan, P, Gould, TD, Li, J, Du, J, Zhang, L, Manji, HK, Chen, G (2003). The role of the extracellular signal-regulated kinase signaling pathway in mood modulation. Journal of Neuroscience 23, 7311–7316.CrossRefGoogle ScholarPubMed
Ellison-Wright, I, Bullmore, E (2010). Anatomy of bipolar disorder and schizophrenia: a meta-analysis. Schizophrenia Research 117, 1–12.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1994). Structured Clinical Interview for DSM-IV Axis I Disorders – Patient Version (SCID-P). American Psychiatric Press: Washington, DC.Google Scholar
Fischl, B, Dale, AM (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences USA 97, 11050–11055.CrossRefGoogle ScholarPubMed
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 (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355.CrossRefGoogle ScholarPubMed
Foland-Ross, LC, Thompson, PM, Sugar, CA, Madsen, SK, Shen, JK, Penfold, C, Ahlf, K, Rasser, PE, Fischer, J, Yang, Y, Townsend, J, Bookheimer, SY, Altshuler, LL (2011). Investigation of cortical thickness abnormalities in lithium-free adults with bipolar I disorder using cortical pattern matching. American Journal of Psychiatry 168, 530–539.CrossRefGoogle ScholarPubMed
Goldman, AL, Pezawas, L, Doz, P, Mattay, VS, Fischl, B, Verchinski, BA, Chen, Q, Weinberger, DR, Meyer-Lindenberg, A (2009). Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. Archives of General Psychiatry 66, 467–477.CrossRefGoogle ScholarPubMed
Greenstein, D, Lerch, J, Shaw, P, Clasen, L, Giedd, J, Gochman, P, Rapoport, J, Gogtay, N (2006). Childhood onset schizophrenia: cortical brain abnormalities as young adults. Journal of Child Psychology and Psychiatry and Allied Disciplines 47, 1003–1012.CrossRefGoogle ScholarPubMed
Hajek, T, Kopecek, M, Kozeny, J, Gunde, E, Alda, M, Höschl, C (2009). Amygdala volumes in mood disorders – meta-analysis of magnetic resonance volumetry studies. Journal of Affective Disorders 115, 395–410.CrossRefGoogle ScholarPubMed
Hall, RC (1995). Global assessment of functioning. A modified scale. Psychosomatics 36, 267–275.CrossRefGoogle ScholarPubMed
Hall, J, Whalley, HC, Marwick, K, McKirdy, J, Sussmann, J, Romaniuk, L, Johnstone, EC, Wan, HI, McIntosh, AM, Lawrie, SM (2010). Hippocampal function in schizophrenia and bipolar disorder. Psychological Medicine 40, 761–770.CrossRefGoogle ScholarPubMed
Hallahan, B, Newell, J, Soares, JC, Brambilla, P, Strakowski, SM, Fleck, DE, Kieseppa, T, Altshuler, LL, Fornito, A, Malhi, GS, McIntosh, AM, Yurgelun-Todd, DA, Labar, KS, Sharma, V, MacQueen, GM, Murray, RM, McDonald, C (2011). Structural magnetic resonance imaging in bipolar disorder: an international collaborative mega-analysis of individual adult patient data. Biological Psychiatry 69, 326–335.CrossRefGoogle ScholarPubMed
Hao, Y, Creson, T, Zhang, L, Li, P, Du, F, Yuan, P, Gould, TD, Manji, HK, Chen, G (2004). Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis. Journal of Neuroscience 24, 6590–6599.CrossRefGoogle ScholarPubMed
Hill, SK, Reilly, JL, Harris, MSH, Rosen, C, Marvin, RW, DeLeon, O, Sweeney, JA (2009). A comparison of neuropsychological dysfunction in first-episode psychosis patients with unipolar depression, bipolar disorder, and schizophrenia. Schizophrenia Research 113, 167–175.CrossRefGoogle ScholarPubMed
Ho, BC, Magnotta, V (2010). Hippocampal volume deficits and shape deformities in young biological relatives of schizophrenia probands. NeuroImage 49, 3385–3393.CrossRefGoogle ScholarPubMed
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle ScholarPubMed
Killgore, WDS, Rosso, IM, Gruber, SA, Yurgelun-Todd, DA (2009). Amygdala volume and verbal memory performance in schizophrenia and bipolar disorder. Cognitive and Behavioral Neurology 22, 28–37.CrossRefGoogle ScholarPubMed
Lichtenstein, P, Yip, BH, Björk, C, Pawitan, Y, Cannon, TD, Sullivan, PF, Hultman, CM (2009). Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study. Lancet 373, 234–239.CrossRefGoogle ScholarPubMed
Lyoo, IK, Sung, YH, Dager, SR, Friedman, SD, Lee, JY, Kim, SJ, Kim, N, Dunner, DL, Renshaw, PF (2006). Regional cerebral cortical thinning in bipolar disorder. Bipolar Disorders 8, 65–74.CrossRefGoogle ScholarPubMed
Möller, HJ (2003). Bipolar disorder and schizophrenia: distinct illnesses or a continuum? Journal of Clinical Psychiatry 64, 23–27.Google ScholarPubMed
Murray, RM, Sham, P, van Os, J, Zanelli, J, Cannon, M, McDonald, C (2004). A developmental model for similarities and dissimilarities between schizophrenia and bipolar disorder. Schizophrenia Research 71, 405–416.CrossRefGoogle ScholarPubMed
Pantelis, C, Velakoulis, D, McGorry, PD, Wood, SJ, Suckling, J, Phillips, LJ, Yung, AR, Bullmore, ET, Brewer, W, Soulsby, B, Desmond, P, McGuire, PK (2003). Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet 361, 281–288.CrossRefGoogle ScholarPubMed
Pearlson, GD, Barta, PE, Powers, RE, Menon, RR, Richards, SS, Aylward, EH, Federman, EB, Chase, GA, Petty, RG, Tien, AY (1997). Medial and superior temporal gyral volumes and cerebral asymmetry in schizophrenia versus bipolar disorder. Biological Psychiatry 41, 1–14.CrossRefGoogle ScholarPubMed
Qiu, A, Brown, T, Fischl, B, Ma, J, Miller, MI (2010 a). Atlas generation for subcortical and ventricular structures with its applications in shape analysis. IEEE Transactions on Image Processing 19, 1539–1547.CrossRefGoogle ScholarPubMed
Qiu, A, Miller, MI (2008). Multi-structure network shape analysis via normal surface momentum maps. NeuroImage 42, 1430–1438.CrossRefGoogle ScholarPubMed
Qiu, A, Tuan, TA, Woon, PS, Abdul-Rahman, MF, Graham, S, Sim, K (2010 b). Hippocampal-cortical structural connectivity disruptions in schizophrenia: an integrated perspective from hippocampal shape, cortical thickness, and integrity of white matter bundles. NeuroImage 52, 1181–1189.CrossRefGoogle ScholarPubMed
Rimol, LM, Hartberg, CB, Nesvåg, R, Fennema-Notestine, C, Hagler, Jr. DJ, Pung, CJ, Jennings, RG, Haukvik, UK, Lange, E, Nakstad, PH, Melle, I, Andreassen, OA, Dale, AM, Agartz, I (2010). Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biological Psychiatry 68, 41–50.CrossRefGoogle ScholarPubMed
Rosso, IM, Killgore, WDS, Cintron, CM, Gruber, SA, Tohen, M, Yurgelun-Todd, DA (2007). Reduced amygdala volumes in first-episode bipolar disorder and correlation with cerebral white matter. Biological Psychiatry 61, 743–749.CrossRefGoogle ScholarPubMed
Sassi, RB, Nicoletti, M, Brambilla, P, Mallinger, AG, Frank, E, Kupfer, DJ, Keshavan, MS, Soares, JC (2002). Increased gray matter volume in lithium-treated bipolar disorder patients. Neuroscience Letters 329, 243–245.CrossRefGoogle ScholarPubMed
Schultz, CC, Koch, K, Wagner, G, Roebel, M, Nenadic, I, Schachtzabel, C, Reichenbach, JR, Sauer, H, Schlösser, RGM (2010). Complex pattern of cortical thinning in schizophrenia: results from an automated surface based analysis of cortical thickness. Psychiatry Research 182, 134–140.CrossRefGoogle ScholarPubMed
Shenton, ME, Gerig, G, McCarley, RW, Székely, G, Kikinis, R (2002). Amygdala-hippocampal shape differences in schizophrenia: the application of 3D shape models to volumetric MR data. Psychiatry Research 115, 15–35.CrossRefGoogle ScholarPubMed
Shepherd, AM, Laurens, KR, Matheson, SL, Carr, VJ, Green, MJ (2012). Systematic meta-review and quality assessment of the structural brain alterations in schizophrenia. Neuroscience and Biobehavioral Reviews 36, 1342–1356.CrossRefGoogle ScholarPubMed
Strasser, HC, Lilyestrom, J, Ashby, ER, Honeycutt, NA, Schretlen, DJ, Pulver, AE, Hopkins, RO, Depaulo, JR, Potash, JB, Schweizer, B, Yates, KO, Kurian, E, Barta, PE, Pearlson, GD (2005). Hippocampal and ventricular volumes in psychotic and nonpsychotic bipolar patients compared with schizophrenia patients and community control subjects: a pilot study. Biological Psychiatry 57, 633–639.CrossRefGoogle ScholarPubMed
Styner, M, Lieberman, JA, Pantazis, D, Gerig, G (2004). Boundary and medial shape analysis of the hippocampus in schizophrenia. Medical Image Analysis 8, 197–203.CrossRefGoogle ScholarPubMed
Suzuki, M, Zhou, SY, Hagino, H, Niu, L, Takahashi, T, Kawasaki, Y, Matsui, M, Seto, H, Ono, T, Kurachi, M (2005). Morphological brain changes associated with Schneider's first-rank symptoms in schizophrenia: a MRI study. Psychological Medicine 35, 549–560.CrossRefGoogle ScholarPubMed
Tanskanen, P, Ridler, K, Graham, KM, Haapea, M, Veijola, JM, Jääskeläinen, E, Miettunen, J, Jones, PB, Bullmore, ET, Isohanni, MK (2010). Morphometric brain abnormalities in schizophrenia in a population-based sample: relationship to duration of illness. Schizophrenia Bulletin 36, 766–777.CrossRefGoogle Scholar
Tracy, JI, Mattson, R, King, C, Bundick, T, Celenza, MA, Glosser, G (2001). A comparison of memory for verbal and non-verbal material in schizophrenia. Schizophrenia Research 50, 199–211.CrossRefGoogle ScholarPubMed
Vaillant, M, Qiu, A, Glaunès, J, Miller, MI (2007). Diffeomorphic metric surface mapping in subregion of the superior temporal gyrus. NeuroImage 34, 1149–1159.CrossRefGoogle ScholarPubMed
van Haren, NEM, Schnack, HG, Cahn, W, van den Heuvel, MP, Lepage, C, Collins, L, Evans, AC, Hulshoff Pol, HE, Kahn, RS (2011). Changes in cortical thickness during the course of illness in schizophrenia. Archives of General Psychiatry 68, 871–880.CrossRefGoogle ScholarPubMed
Velakoulis, D, Wood, SJ, Wong, MTH, McGorry, PD, Yung, A, Phillips, L, Smith, D, Brewer, W, Proffitt, T, Desmond, P, Pantelis, C (2006). Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, first-episode psychosis, and ultra-high-risk individuals. Archives of General Psychiatry 63, 139–149.CrossRefGoogle ScholarPubMed
Wang, KS, Liu, XF, Aragam, N (2010). A genome-wide meta-analysis identifies novel loci associated with schizophrenia and bipolar disorder. Schizophrenia Research 124, 192–199.CrossRefGoogle ScholarPubMed
Witthaus, H, Kaufmann, C, Bohner, G, Özgürdal, S, Gudlowski, Y, Gallinat, J, Ruhrmann, S, Brüne, M, Heinz, A, Klingebiel, R, Juckel, G (2009). Gray matter abnormalities in subjects at ultra-high risk for schizophrenia and first-episode schizophrenic patients compared to healthy controls. Psychiatry Research 173, 163–169.CrossRefGoogle ScholarPubMed
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429–435.CrossRefGoogle ScholarPubMed
Yucel, K, McKinnon, MC, Taylor, VH, Macdonald, K, Alda, M, Young, LT, MacQueen, GM (2007). Bilateral hippocampal volume increases after long-term lithium treatment in patients with bipolar disorder: a longitudinal MRI study. Psychopharmacology 195, 357–367.CrossRefGoogle ScholarPubMed
Zhong, J, Phua, DY, Qiu, A (2010). Quantitative evaluation of LDDMM, FreeSurfer, and CARET for cortical surface mapping. NeuroImage 52, 131–141.CrossRefGoogle ScholarPubMed
Zhong, J, Qiu, A (2010). Multi-manifold diffeomorphic metric mapping for aligning cortical hemispheric surfaces. NeuroImage 49, 355–365.CrossRefGoogle ScholarPubMed
Zipursky, RB, Seeman, MV, Bury, A, Langevin, R, Wortzman, G, Katz, R (1997). Deficits in gray matter volume are present in schizophrenia but not bipolar disorder. Schizophrenia Research 26, 85–92.CrossRefGoogle Scholar
Supplementary material: File

Qiu et al. supplementary material

Supplementary figures

Download Qiu et al. supplementary material(File)
File 66.1 MB