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Dentate gyrus volume deficit in schizophrenia

Published online by Cambridge University Press:  03 June 2019

Soichiro Nakahara ,
Jessica A. Turner ,
Vince D. Calhoun ,
Kelvin O. Lim ,
Bryon Mueller ,
Juan R. Bustillo ,
Daniel S. O'Leary ,
Sarah McEwen ,
James Voyvodic  and
Aysenil Belger
...Show all authors
Soichiro Nakahara
Affiliation:
Clinical Translational Neuroscience Laboratory, Department of Psychiatry and Human Behavior, University of California Irvine, Irvine, CA92617, USA Virtual Venture Unit, Psychiatry, Drug Discovery Research, Astellas Pharma Inc., 21, Miyukigaoka, Tsukuba, Ibaraki305-8585, Japan
Jessica A. Turner
Affiliation:
The Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS) {Georgia State, Georgia Tech, Emory}, Atlanta, GA30300, USA Departments of Psychology and Neuroscience, Georgia State University, Atlanta, GA30302, USA Mind Research Network, Albuquerque, NM87106, USA
Vince D. Calhoun
Affiliation:
The Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS) {Georgia State, Georgia Tech, Emory}, Atlanta, GA30300, USA Mind Research Network, Albuquerque, NM87106, USA Department of Electrical and Computer Engineering, University of New Mexico, Albuquerque, NM87131, USA Departments of Psychiatry & Neuroscience, University of New Mexico, Albuquerque, NM87131, USA
Kelvin O. Lim
Affiliation:
Department of Psychiatry, University of Minnesota, Minneapolis, MN55454, USA
Bryon Mueller
Affiliation:
Department of Psychiatry, University of Minnesota, Minneapolis, MN55454, USA
Juan R. Bustillo
Affiliation:
Departments of Psychiatry & Neuroscience, University of New Mexico, Albuquerque, NM87131, USA
Daniel S. O'Leary
Affiliation:
Department of Psychiatry, University of Iowa, Iowa City, IA52242, USA
Sarah McEwen
Affiliation:
Department of Psychiatry, University of California, San Diego, La Jolla, CA92093, USA
James Voyvodic
Affiliation:
Brain Imaging and Analysis Center, Duke University Medical Center, Durham, NC27710, USA
Aysenil Belger
Affiliation:
Department of Psychiatry, University of North Carolina at Chapel Hill, Chapel Hill, NC27599, USA
Daniel H. Mathalon
Affiliation:
Department of Psychiatry, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA94143, USA Veterans Affairs San Francisco Healthcare System, San Francisco, CA94121, USA
Judith M. Ford
Affiliation:
Department of Psychiatry, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA94143, USA Veterans Affairs San Francisco Healthcare System, San Francisco, CA94121, USA
Fabio Macciardi
Affiliation:
Department of Psychiatry and Human Behavior, University of California Irvine, Irvine, CA92617, USA
Mitsuyuki Matsumoto
Affiliation:
Virtual Venture Unit, Psychiatry, Drug Discovery Research, Astellas Pharma Inc., 21, Miyukigaoka, Tsukuba, Ibaraki305-8585, Japan
Steven G. Potkin
Affiliation:
Department of Psychiatry and Human Behavior, University of California Irvine, Irvine, CA92617, USA
Theo G. M. van Erp*
Affiliation:
Clinical Translational Neuroscience Laboratory, Department of Psychiatry and Human Behavior, University of California Irvine, Irvine, CA92617, USA Center for the Neurobiology of Learning and Memory, University of California Irvine, Irvine, CA92697, USA
*
Author for correspondence: Theo G. M. van Erp, E-mail: [email protected]
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Abstract

Background

Schizophrenia is associated with robust hippocampal volume deficits but subregion volume deficits, their associations with cognition, and contributing genes remain to be determined.

Methods

Hippocampal formation (HF) subregion volumes were obtained using FreeSurfer 6.0 from individuals with schizophrenia (n = 176, mean age ± s.d. = 39.0 ± 11.5, 132 males) and healthy volunteers (n = 173, mean age ± s.d. = 37.6 ± 11.3, 123 males) with similar mean age, gender, handedness, and race distributions. Relationships between the HF subregion volume with the largest between group difference, neuropsychological performance, and single-nucleotide polymorphisms were assessed.

Results

This study found a significant group by region interaction on hippocampal subregion volumes. Compared to healthy volunteers, individuals with schizophrenia had significantly smaller dentate gyrus (DG) (Cohen's d = −0.57), Cornu Ammonis (CA) 4, molecular layer of the hippocampus, hippocampal tail, and CA 1 volumes, when statistically controlling for intracranial volume; DG (d = −0.43) and CA 4 volumes remained significantly smaller when statistically controlling for mean hippocampal volume. DG volume showed the largest between group difference and significant positive associations with visual memory and speed of processing in the overall sample. Genome-wide association analysis with DG volume as the quantitative phenotype identified rs56055643 (β = 10.8, p < 5 × 10−8, 95% CI 7.0–14.5) on chromosome 3 in high linkage disequilibrium with MOBP. Gene-based analyses identified associations between SLC25A38 and RPSA and DG volume.

Conclusions

This study suggests that DG dysfunction is fundamentally involved in schizophrenia pathophysiology, that it may contribute to cognitive abnormalities in schizophrenia, and that underlying biological mechanisms may involve contributions from MOBP, SLC25A38, and RPSA.

Keywords

geneticsgenome-wide association analysishippocampusimagingsubfield
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 8 , June 2020 , pp. 1267 - 1277
Copyright
Copyright © Cambridge University Press 2019

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References

Adler, DH, Pluta, J, Kadivar, S, Craige, C, Gee, JC, Avants, BB and Yushkevich, PA (2014) Histology-derived volumetric annotation of the human hippocampal subfields in postmortem MRI. NeuroImage 84, 505–523.CrossRefGoogle ScholarPubMed
Amaral, DG and Witter, MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571–591.CrossRefGoogle ScholarPubMed
Amaral, DG, Scharfman, HE and Lavenex, P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Progress in Brain Research 216, 3–22.Google Scholar
Baglivo, V, Cao, B, Mwangi, B, Bellani, M, Perlini, C, Lasalvia, A, Dusi, N, Bonetto, C, Cristofalo, D, Alessandrini, F, Zoccatelli, G, Ciceri, E, Dario, L, Enrico, C, Francesca, P, Mazzi, F, Paolo, S, Balestrieri, M, Soares, JC, Ruggeri, M and Brambilla, P, GET UP Group (2017) Hippocampal subfield volumes in patients with first-episode psychosis. Schizophrenia Bulletin 44, 552–559.CrossRefGoogle Scholar
Barsh, GS, Copenhaver, GP, Gibson, G and Williams, SM (2012) Guidelines for genome-wide association studies. PLoS Genetics 8, e1002812.CrossRefGoogle ScholarPubMed
Boedhoe, PSW, Schmaal, L, Abe, Y, Ameis, SH, Arnold, PD, Batistuzzo, MC, Benedetti, F, Beucke, JC, Bollettini, I, Bose, A, Brem, S, Calvo, A, Cheng, Y, Cho, KIK, Dallaspezia, S, Denys, D, Fitzgerald, KD, Fouche, J-P, Giménez, M, Gruner, P, Hanna, GL, Hibar, DP, Hoexter, MQ, Hu, H, Huyser, C, Ikari, K, Jahanshad, N, Kathmann, N, Kaufmann, C, Koch, K, Kwon, JS, Lazaro, L, Liu, Y, Lochner, C, Marsh, R, Martínez-Zalacaín, I, Mataix-Cols, D, Menchón, JM, Minuzzi, L, Nakamae, T, Nakao, T, Narayanaswamy, JC, Piras, F, Piras, F, Pittenger, C, Reddy, YCJ, Sato, JR, Simpson, HB, Soreni, N, Soriano-Mas, C, Spalletta, G, Stevens, MC, Szeszko, PR, Tolin, DF, Venkatasubramanian, G, Walitza, S, Wang, Z, van Wingen, GA, Xu, J, Xu, X, Yun, J-Y, Zhao, Q, ENIGMA OCD Working Group, Thompson, PM, Stein, DJ and van den Heuvel, OA (2017) Distinct subcortical volume alterations in pediatric and adult OCD: a worldwide meta- and mega-analysis. The American Journal of Psychiatry 174, 60–69.CrossRefGoogle ScholarPubMed
Carter, CS, Bearden, CE, Bullmore, ET, Geschwind, DH, Glahn, DC, Gur, RE, Meyer-Lindenberg, A and Weinberger, DR (2017) Enhancing the informativeness and replicability of imaging genomics studies. Biological Psychiatry 82, 157–164.CrossRefGoogle ScholarPubMed
Chambers, JS and Perrone-Bizzozero, NI (2004) Altered myelination of the hippocampal formation in subjects with schizophrenia and bipolar disorder. Neurochemical Research 29, 2293–2302.CrossRefGoogle ScholarPubMed
Chatzi, C, Zhang, Y, Shen, R, Westbrook, GL and Goodman, RH (2016) Transcriptional profiling of newly generated dentate granule cells using TU tagging reveals pattern shifts in gene expression during circuit integration. eNeuro 3, 1–17.CrossRefGoogle ScholarPubMed
Das, S, Forer, L, Schönherr, S, Sidore, C, Locke, AE, Kwong, A, Vrieze, SI, Chew, EY, Levy, S, McGue, M, Schlessinger, D, Stambolian, D, Loh, P-R, Iacono, WG, Swaroop, A, Scott, LJ, Cucca, F, Kronenberg, F, Boehnke, M, Abecasis, GR and Fuchsberger, C (2016) Next-generation genotype imputation service and methods. Nature Genetics 48, 1284–1287.CrossRefGoogle ScholarPubMed
de Belmont Hollingshead, A (1975) Four Factor Index of Social Status. Unpublished Working Paper, Yale University, New Haven, CT.Google Scholar
Durazzo, TC, Pennington, DL, Schmidt, TP, Mon, A, Abé, C and Meyerhoff, DJ (2013) Neurocognition in 1-month-abstinent treatment-seeking alcohol-dependent individuals: interactive effects of age and chronic cigarette smoking. Alcoholism, Clinical and Experimental Research 37, 1794–1803.Google ScholarPubMed
Esteban, O, Birman, D, Schaer, M, Koyejo, OO, Poldrack, RA and Gorgolewski, KJ (2017) MRIQC: advancing the automatic prediction of image quality in MRI from unseen sites. PLoS ONE 12, e0184661.CrossRefGoogle ScholarPubMed
Fennema-Notestine, C, Gamst, AC, Quinn, BT, Pacheco, J, Jernigan, TL, Thal, L, Buckner, R, Killiany, R, Blacker, D, Dale, AM, Fischl, B, Dickerson, B and Gollub, RL (2007) Feasibility of multi-site clinical structural neuroimaging studies of aging using legacy data. Neuroinformatics 5, 235–245.CrossRefGoogle ScholarPubMed
First, MB (2002) User's Guide for the Structured Clinical Interview for DSM-IV-TR Axis I Disorders: SCID-I. Washington DC: American Psychiatric Press, Inc.Google Scholar
Fischl, B (2012) Freesurfer. NeuroImage 62, 774–781.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 and Dale, AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355.CrossRefGoogle ScholarPubMed
Francis, AN, Seidman, LJ, Tandon, N, Shenton, ME, Thermenos, HW, Mesholam-Gately, RI, van Elst, LT, Tuschen-Caffier, B, DeLisi, LE and Keshavan, MS (2013) Reduced subicular subdivisions of the hippocampal formation and verbal declarative memory impairments in young relatives at risk for schizophrenia. Schizophrenia Research 151, 154–157.CrossRefGoogle ScholarPubMed
Friedman, L and Glover, GH (2006) Report on a multicenter fMRI quality assurance protocol. Journal of Magnetic Resonance Imaging 23, 827–839.CrossRefGoogle ScholarPubMed
Friedman, L, Glover, GH and Fbirn Consortium (2006) Reducing interscanner variability of activation in a multicenter fMRI study: controlling for signal-to-fluctuation-noise-ratio (SFNR) differences. NeuroImage 33, 471–481.CrossRefGoogle Scholar
Glover, GH, Mueller, BA, Turner, JA, van Erp, TGM, Liu, TT, Greve, DN, Voyvodic, JT, Rasmussen, J, Brown, GG, Keator, DB, Calhoun, VD, Lee, HJ, Ford, JM, Mathalon, DH, Diaz, M, O'Leary, DS, Gadde, S, Preda, A, Lim, KO, Wible, CG, Stern, HS, Belger, A, McCarthy, G, Ozyurt, B and Potkin, SG (2012) Function biomedical informatics research network recommendations for prospective multicenter functional MRI studies. Journal of Magnetic Resonance Imaging: JMRI 36, 39–54.CrossRefGoogle ScholarPubMed
Greenspan, KS, Arakelian, CR and van Erp, TGM (2016) Heritability of hippocampal formation sub-region volumes. Journal of Neurology and Neuroscience 7, 1–7.CrossRefGoogle ScholarPubMed
Greve, DN, Mueller, BA, Liu, T, Turner, JA, Voyvodic, J, Yetter, E, Diaz, M, McCarthy, G, Wallace, S, Roach, BJ, Ford, JM, Mathalon, DH, Calhoun, VD, Wible, CG, Brown, GG, Potkin, SG and Glover, G (2011) A novel method for quantifying scanner instability in fMRI. Magnetic Resonance in Medicine 65, 1053–1061.CrossRefGoogle ScholarPubMed
Hagihara, H, Takao, K, Walton, NM, Matsumoto, M and Miyakawa, T (2013) Immature dentate gyrus: an endophenotype of neuropsychiatric disorders. Neural Plasticity 2013, 318596.CrossRefGoogle ScholarPubMed
Haijma, SV, Van Haren, N, Cahn, W, Koolschijn, PCMP, Hulshoff Pol, HE and Kahn, RS (2013) Brain volumes in schizophrenia: a meta-analysis in over 18 000 subjects. Schizophrenia Bulletin 39, 1129–1138.CrossRefGoogle ScholarPubMed
Hancock, DB, Soler Artigas, M, Gharib, SA, Henry, A, Manichaikul, A, Ramasamy, A, Loth, DW, Imboden, M, Koch, B, McArdle, WL, Smith, AV, Smolonska, J, Sood, A, Tang, W, Wilk, JB, Zhai, G, Zhao, JH, Aschard, H, Burkart, KM, Curjuric, I, Eijgelsheim, M, Elliott, P, Gu, X, Harris, TB, Janson, C, Homuth, G, Hysi, PG, Liu, JZ, Loehr, LR, Lohman, K, Loos, RJF, Manning, AK, Marciante, KD, Obeidat, M, Postma, DS, Aldrich, MC, Brusselle, GG, Chen, T-H, Eiriksdottir, G, Franceschini, N, Heinrich, J, Rotter, JI, Wijmenga, C, Williams, OD, Bentley, AR, Hofman, A, Laurie, CC, Lumley, T, Morrison, AC, Joubert, BR, Rivadeneira, F, Couper, DJ, Kritchevsky, SB, Liu, Y, Wjst, M, Wain, LV, Vonk, JM, Uitterlinden, AG, Rochat, T, Rich, SS, Psaty, BM, O'Connor, GT, North, KE, Mirel, DB, Meibohm, B, Launer, LJ, Khaw, K-T, Hartikainen, A-L, Hammond, CJ, Gläser, S, Marchini, J, Kraft, P, Wareham, NJ, Völzke, H, Stricker, BHC, Spector, TD, Probst-Hensch, NM, Jarvis, D, Jarvelin, M-R, Heckbert, SR, Gudnason, V, Boezen, HM, Barr, RG, Cassano, PA, Strachan, DP, Fornage, M, Hall, IP, Dupuis, J, Tobin, MD and London, SJ (2012) Genome-wide joint meta-analysis of SNP and SNP-by-smoking interaction identifies novel loci for pulmonary function. PLoS Genetics 8, e1003098.CrossRefGoogle ScholarPubMed
Haukvik, UK, Westlye, LT, Mørch-Johnsen, L, Jørgensen, KN, Lange, EH, Dale, AM, Melle, I, Andreassen, OA and Agartz, I (2015) In vivo hippocampal subfield volumes in schizophrenia and bipolar disorder. Biological Psychiatry 77, 581–588.CrossRefGoogle ScholarPubMed
Haukvik, UK, Tamnes, CK, Söderman, E and Agartz, I (2018) Neuroimaging hippocampal subfields in schizophrenia and bipolar disorder: a systematic review and meta-analysis. Journal of Psychiatric Research 104, 217–226.CrossRefGoogle ScholarPubMed
Hegyi, H (2017) Connecting myelin-related and synaptic dysfunction in schizophrenia with SNP-rich gene expression hubs. Scientific Reports 7, 45494.CrossRefGoogle ScholarPubMed
Ho, NF, Holt, DJ, Cheung, M, Iglesias, JE, Goh, A, Wang, M, Lim, JK, de Souza, J, Poh, JS, See, YM, Adcock, AR, Wood, SJ, Chee, MW, Lee, J and Zhou, J (2017a) Progressive decline in hippocampal CA1 volume in individuals at ultra-high-risk for psychosis who do not remit: findings from the longitudinal youth at risk study. Neuropsychopharmacology 42, 1361–1370.CrossRefGoogle Scholar
Ho, NF, Iglesias, JE, Sum, MY, Kuswanto, CN, Sitoh, YY, De Souza, J, Hong, Z, Fischl, B, Roffman, JL, Zhou, J, Sim, K and Holt, DJ (2017b) Progression from selective to general involvement of hippocampal subfields in schizophrenia. Molecular Psychiatry 22, 142–152.CrossRefGoogle Scholar
Höglinger, GU, Melhem, NM, Dickson, DW, Sleiman, PMA, Wang, L-S, Klei, L, Rademakers, R, de Silva, R, Litvan, I, Riley, DE, van Swieten, JC, Heutink, P, Wszolek, ZK, Uitti, RJ, Vandrovcova, J, Hurtig, HI, Gross, RG, Maetzler, W, Goldwurm, S, Tolosa, E, Borroni, B, Pastor, P, PSP Genetics Study Group, Cantwell, LB, Han, MR, Dillman, A, van der Brug, MP, Gibbs, JR, Cookson, MR, Hernandez, DG, Singleton, AB, Farrer, MJ, Yu, C-E, Golbe, LI, Revesz, T, Hardy, J, Lees, AJ, Devlin, B, Hakonarson, H, Müller, U and Schellenberg, GD (2011) Identification of common variants influencing risk of the tauopathy progressive supranuclear palsy. Nature Genetics 43, 699–705.CrossRefGoogle ScholarPubMed
Hýža, M, Kuhn, M, Češková, E, Ustohal, L and Kašpárek, T (2016) Hippocampal volume in first-episode schizophrenia and longitudinal course of the illness. The World Journal of Biological Psychiatry 17, 429–438.CrossRefGoogle ScholarPubMed
Iglesias, JE, Sabuncu, MR and Van Leemput, K, Alzheimer's Disease Neuroimaging Initiative (2013) Improved inference in Bayesian segmentation using Monte Carlo sampling: application to hippocampal subfield volumetry. Medical Image Analysis 17, 766–778.CrossRefGoogle ScholarPubMed
Kawano, M, Sawada, K, Shimodera, S, Ogawa, Y, Kariya, S, Lang, DJ, Inoue, S and Honer, WG (2015) Hippocampal subfield volumes in first episode and chronic schizophrenia. PLoS ONE 10, e0117785.CrossRefGoogle ScholarPubMed
Kay, SR, Opler, LA and Lindenmayer, J-P (1989) The positive and negative syndrome scale (PANSS): rationale and standardisation. British Journal of Psychiatry 155, 59–65.CrossRefGoogle Scholar
Kubicki, M, McCarley, RW and Shenton, ME (2005) Evidence for white matter abnormalities in schizophrenia. Current Opinion in Psychiatry 18, 121–134.CrossRefGoogle Scholar
Mathew, I, Gardin, TM, Tandon, N, Eack, S, Francis, AN, Seidman, LJ, Clementz, B, Pearlson, GD, Sweeney, JA, Tamminga, CA and Keshavan, MS (2014) Medial temporal lobe structures and hippocampal subfields in psychotic disorders: findings from the Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP) study. JAMA Psychiatry 71, 769–777.CrossRefGoogle ScholarPubMed
McInnes, LA and Lauriat, TL (2006) RNA metabolism and dysmyelination in schizophrenia. Neuroscience and Biobehavioral Reviews 30, 551–561.CrossRefGoogle Scholar
Nakahara, S, Matsumoto, M and van Erp, TGM (2018) Hippocampal subregion abnormalities in schizophrenia: a systematic review of structural and physiological imaging studies. Neuropsychopharmacology Reports 38, 156–166.CrossRefGoogle ScholarPubMed
Ohira, K, Kobayashi, K, Toyama, K, Nakamura, HK, Shoji, H, Takao, K, Takeuchi, R, Yamaguchi, S, Kataoka, M, Otsuka, S, Takahashi, M and Miyakawa, T (2013) Synaptosomal-associated protein 25 mutation induces immaturity of the dentate granule cells of adult mice. Molecular Brain 6, 12.CrossRefGoogle ScholarPubMed
Okada, N, Fukunaga, M, Yamashita, F, Koshiyama, D, Yamamori, H, Ohi, K, Yasuda, Y, Fujimoto, M, Watanabe, Y, Yahata, N, Nemoto, K, Hibar, DP, van Erp, TGM, Fujino, H, Isobe, M, Isomura, S, Natsubori, T, Narita, H, Hashimoto, N, Miyata, J, Koike, S, Takahashi, T, Yamasue, H, Matsuo, K, Onitsuka, T, Iidaka, T, Kawasaki, Y, Yoshimura, R, Watanabe, Y, Suzuki, M, Turner, JA, Takeda, M, Thompson, PM, Ozaki, N, Kasai, K and Hashimoto, R (2016) Abnormal asymmetries in subcortical brain volume in schizophrenia. Molecular Psychiatry 21, 1460–1466.CrossRefGoogle Scholar
Oldfield, RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Omar, MH, Campbell, MK, Xiao, X, Zhong, Q, Brunken, WJ, Miner, JH, Greer, CA and Koleske, AJ (2017) CNS neurons deposit Laminin α5 to stabilize synapses. Cell Reports 21, 1281–1292.CrossRefGoogle ScholarPubMed
Ota, M, Sato, N, Hidese, S, Teraishi, T, Maikusa, N, Matsuda, H, Hattori, K and Kunugi, H (2017) Structural differences in hippocampal subfields among schizophrenia patients, major depressive disorder patients, and healthy subjects. Psychiatry Research 259, 54–59.CrossRefGoogle ScholarPubMed
Purcell, S, Neale, B, Todd-Brown, K, Thomas, L, Ferreira, MAR, Bender, D, Maller, J, Sklar, P, de Bakker, PIW, Daly, MJ and Sham, PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics 81, 559–575.CrossRefGoogle ScholarPubMed
Rhindress, K, Robinson, DG, Gallego, JA, Wellington, R, Malhotra, AK and Szeszko, PR (2017) Hippocampal subregion volume changes associated with antipsychotic treatment in first-episode psychosis. Psychological Medicine 47, 1706–1718.CrossRefGoogle ScholarPubMed
Risch, N and Merikangas, K (1996) The future of genetic studies of complex human diseases. Science 273, 1516–1517.CrossRefGoogle ScholarPubMed
Sauras, R, Keymer, A, Alonso-Solis, A, Díaz, A, Molins, C, Nuñez, F, Rabella, M, Roldán, A, Grasa, E, Alvarez, E, Portella, MJ and Corripio, I (2017) Volumetric and morphological characteristics of the hippocampus are associated with progression to schizophrenia in patients with first-episode psychosis. European Psychiatry: The Journal of the Association of European Psychiatrists 45, 1–5.CrossRefGoogle ScholarPubMed
Schmitt, A, Steyskal, C, Bernstein, H-G, Schneider-Axmann, T, Parlapani, E, Schaeffer, EL, Gattaz, WF, Bogerts, B, Schmitz, C and Falkai, P (2009) Stereologic investigation of the posterior part of the hippocampus in schizophrenia. Acta Neuropathologica 117, 395–407.CrossRefGoogle Scholar
Schneider, CE, White, T, Hass, J, Geisler, D, Wallace, SR, Roessner, V, Holt, DJ, Calhoun, VD, Gollub, RL and Ehrlich, S (2014) Smoking status as a potential confounder in the study of brain structure in schizophrenia. Journal of Psychiatric Research 50, 84–91.CrossRefGoogle Scholar
Schobel, SA, Lewandowski, NM, Corcoran, CM, Moore, H, Brown, T, Malaspina, D and Small, SA (2009) Differential targeting of the CA1 subfield of the hippocampal formation by schizophrenia and related psychotic disorders. Archives of General Psychiatry 66, 938–946.CrossRefGoogle ScholarPubMed
Segall, JM, Turner, JA, van Erp, TGM, White, T, Bockholt, HJ, Gollub, RL, Ho, BC, Magnotta, V, Jung, RE, McCarley, RW, Schulz, SC, Lauriello, J, Clark, VP, Voyvodic, JT, Diaz, MT and Calhoun, VD (2009) Voxel-based morphometric multisite collaborative study on schizophrenia. Schizophrenia Bulletin 35, 82–95.CrossRefGoogle Scholar
Small, SA, Schobel, SA, Buxton, RB, Witter, MP and Barnes, CA (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nature Reviews. Neuroscience 12, 585–601.CrossRefGoogle ScholarPubMed
Steinberg, S, Mors, O, Børglum, AD, Gustafsson, O, Werge, T, Mortensen, PB, Andreassen, OA, Sigurdsson, E, Thorgeirsson, TE, Böttcher, Y, Olason, P, Ophoff, RA, Cichon, S, Gudjonsdottir, IH, Pietiläinen, OPH, Nyegaard, M, Tuulio-Henriksson, A, Ingason, A, Hansen, T, Athanasiu, L, Suvisaari, J, Lonnqvist, J, Paunio, T, Hartmann, A, Jürgens, G, Nordentoft, M, Hougaard, D, Norgaard-Pedersen, B, Breuer, R, Möller, H-J, Giegling, I, Glenthøj, B, Rasmussen, HB, Mattheisen, M, Bitter, I, Réthelyi, JM, Sigmundsson, T, Fossdal, R, Thorsteinsdottir, U, Ruggeri, M, Tosato, S, Strengman, E, Genetic Risk and Outcome in Psychosis, Kiemeney, LA, Melle, I, Djurovic, S, Abramova, L, Kaleda, V, Walshe, M, Bramon, E, Vassos, E, Li, T, Fraser, G, Walker, N, Toulopoulou, T, Yoon, J, Freimer, NB, Cantor, RM, Murray, R, Kong, A, Golimbet, V, Jönsson, EG, Terenius, L, Agartz, I, Petursson, H, Nöthen, MM, Rietschel, M, Peltonen, L, Rujescu, D, Collier, DA, Stefansson, H, St Clair, D and Stefansson, K (2011) Expanding the range of ZNF804A variants conferring risk of psychosis. Molecular Psychiatry 16, 59–66.CrossRefGoogle ScholarPubMed
van Erp, TGM, Greve, DN, Rasmussen, J, Turner, J, Calhoun, VD, Young, S, Mueller, B, Brown, GG, McCarthy, G, Glover, GH, Lim, KO, Bustillo, JR, Belger, A, McEwen, S, Voyvodic, J, Mathalon, DH, Keator, D, Preda, A, Nguyen, D, Ford, JM and Potkin, SG, FBIRN (2014) A multi-scanner study of subcortical brain volume abnormalities in schizophrenia. Psychiatry Research 222, 10–16.CrossRefGoogle Scholar
van Erp, TGM, Preda, A, Turner, JA, Callahan, S, Calhoun, VD, Bustillo, JR, Lim, KO, Mueller, B, Brown, GG, Vaidya, JG, McEwen, S, Belger, A, Voyvodic, J, Mathalon, DH, Nguyen, D, Ford, JM and Potkin, SG, FBIRN (2015) Neuropsychological profile in adult schizophrenia measured with the CMINDS. Psychiatry Research 230, 826–834.CrossRefGoogle ScholarPubMed
van Erp, TGM, Hibar, DP, Rasmussen, JM, Glahn, DC, Pearlson, GD, Andreassen, OA, Agartz, I, Westlye, LT, Haukvik, UK, Dale, AM, Melle, I, Hartberg, CB, Gruber, O, Kraemer, B, Zilles, D, Donohoe, G, Kelly, S, McDonald, C, Morris, DW, Cannon, DM, Corvin, A, Machielsen, MWJ, Koenders, L, de Haan, L, Veltman, DJ, Satterthwaite, TD, Wolf, DH, Gur, RC, Gur, RE, Potkin, SG, Mathalon, DH, Mueller, BA, Preda, A, Macciardi, F, Ehrlich, S, Walton, E, Hass, J, Calhoun, VD, Bockholt, HJ, Sponheim, SR, Shoemaker, JM, van Haren, NEM, Pol, HEH, Ophoff, RA, Kahn, RS, Roiz-Santiañez, R, Crespo-Facorro, B, Wang, L, Alpert, KI, Jönsson, EG, Dimitrova, R, Bois, C, Whalley, HC, McIntosh, AM, Lawrie, SM, Hashimoto, R, Thompson, PM and Turner, JA (2016) Subcortical brain volume abnormalities in 2028 individuals with schizophrenia and 2540 healthy controls via the ENIGMA consortium. Molecular Psychiatry 21, 585.CrossRefGoogle ScholarPubMed
Tamminga, CA, Stan, AD and Wagner, AD (2010) The hippocampal formation in schizophrenia. The American Journal of Psychiatry 167, 1178–1193.CrossRefGoogle Scholar
Tamminga, CA, Southcott, S, Sacco, C, Wagner, AD and Ghose, S (2012) Glutamate dysfunction in hippocampus: relevance of dentate gyrus and CA3 signaling. Schizophrenia Bulletin 38, 927–935.CrossRefGoogle ScholarPubMed
Uttl, B (2002) North American Adult Reading Test: age norms, reliability, and validity. Journal of Clinical and Experimental Neuropsychology 24, 1123–1137.CrossRefGoogle ScholarPubMed
Van Leemput, K, Bakkour, A, Benner, T, Wiggins, G, Wald, LL, Augustinack, J, Dickerson, BC, Golland, P and Fischl, B (2008) Model-based segmentation of hippocampal subfields in ultra-high resolution in vivo MRI. Medical Image Computing and Computer-Assisted Intervention: MICCAI … International Conference on Medical Image Computing and Computer-Assisted Intervention 11, 235–243.Google ScholarPubMed
Van Leemput, K, Bakkour, A, Benner, T, Wiggins, G, Wald, LL, Augustinack, J, Dickerson, BC, Golland, P and Fischl, B (2009) Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 19, 549–557.CrossRefGoogle ScholarPubMed
Walton, NM, Zhou, Y, Kogan, JH, Shin, R, Webster, M, Gross, AK, Heusner, CL, Chen, Q, Miyake, S, Tajinda, K, Tamura, K, Miyakawa, T and Matsumoto, M (2012) Detection of an immature dentate gyrus feature in human schizophrenia/bipolar patients. Translational Psychiatry 2, e135.CrossRefGoogle Scholar
Watanabe, K, Taskesen, E, van Bochoven, A and Posthuma, D (2017) Functional mapping and annotation of genetic associations with FUMA. Nature Communications 8, 1–11.CrossRefGoogle ScholarPubMed
Wheeler, DW, White, CM, Rees, CL, Komendantov, AO, Hamilton, DJ and Ascoli, GA (2015) Hippocampome.org: a knowledge base of neuron types in the rodent hippocampus. eLife 4, 1–28.CrossRefGoogle ScholarPubMed
Whelan, CD, Hibar, DP, van Velzen, LS, Zannas, AS, Carrillo-Roa, T, McMahon, K, Prasad, G, Kelly, S, Faskowitz, J, deZubiracay, G, Iglesias, JE, van Erp, TGM, Frodl, T, Martin, NG, Wright, MJ, Jahanshad, N, Schmaal, L, Sämann, PG and Thompson, PM, Alzheimer's Disease Neuroimaging Initiative (2016) Heritability and reliability of automatically segmented human hippocampal formation subregions. NeuroImage 128, 125–137.CrossRefGoogle ScholarPubMed
Wisse, LEM, Biessels, GJ and Geerlings, MI (2014) A critical appraisal of the hippocampal subfield segmentation package in FreeSurfer. Frontiers in Aging Neuroscience 6, 261.CrossRefGoogle ScholarPubMed
Yushkevich, PA, Avants, BB, Pluta, J, Minkoff, D, Detre, JA, Grossman, M and Gee, JC (2008) Shape-based alignment of hippocampal subfields: evaluation in postmortem MRI. Medical Image Computing and Computer-Assisted Intervention: MICCAI … International Conference on Medical Image Computing and Computer-Assisted Intervention 11, 510–517.Google ScholarPubMed
Yushkevich, PA, Avants, BB, Pluta, J, Das, S, Minkoff, D, Mechanic-Hamilton, D, Glynn, S, Pickup, S, Liu, W, Gee, JC, Grossman, M and Detre, JA (2009) A high-resolution computational atlas of the human hippocampus from postmortem magnetic resonance imaging at 9.4 T. NeuroImage 44, 385–398.CrossRefGoogle ScholarPubMed
Zhang, R, Valenzuela, RK, Lu, S, Meng, L, Guo, T, Du, X, Kang, W and Ma, J (2011) Is the conserved mammalian region of ZNF804A locus associated with schizophrenia? A population-based genetics analysis. Schizophrenia Research 133, 159–164.CrossRefGoogle ScholarPubMed
Zhang, H, Zhang, Y-W, Chen, Y, Huang, X, Zhou, F, Wang, W, Xian, B, Zhang, X, Masliah, E, Chen, Q, Han, J-DJ, Bu, G, Reed, JC, Liao, F-F, Chen, Y-G and Xu, H (2012) Appoptosin is a novel pro-apoptotic protein and mediates cell death in neurodegeneration. The Journal of Neuroscience 32, 15565–15576.CrossRefGoogle ScholarPubMed
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