Skip to main content Accessibility help

Dentate gyrus volume deficit in schizophrenia

  • Soichiro Nakahara (a1) (a2), Jessica A. Turner (a3) (a4) (a5), Vince D. Calhoun (a3) (a5) (a6) (a7), Kelvin O. Lim (a8), Bryon Mueller (a8), Juan R. Bustillo (a7), Daniel S. O'Leary (a9), Sarah McEwen (a10), James Voyvodic (a11), Aysenil Belger (a12), Daniel H. Mathalon (a13) (a14), Judith M. Ford (a13) (a14), Fabio Macciardi (a15), Mitsuyuki Matsumoto (a2), Steven G. Potkin (a15) and Theo G. M. van Erp (a1) (a16)...



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


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.


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.


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.


Corresponding author

Author for correspondence: Theo G. M. van Erp, E-mail:


Hide All
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, 505523.
Amaral, DG and Witter, MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571591.
Amaral, DG, Scharfman, HE and Lavenex, P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Progress in Brain Research 216, 322.
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, 552559.
Barsh, GS, Copenhaver, GP, Gibson, G and Williams, SM (2012) Guidelines for genome-wide association studies. PLoS Genetics 8, e1002812.
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, 6069.
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, 157164.
Chambers, JS and Perrone-Bizzozero, NI (2004) Altered myelination of the hippocampal formation in subjects with schizophrenia and bipolar disorder. Neurochemical Research 29, 22932302.
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, 117.
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, 12841287.
de Belmont Hollingshead, A (1975) Four Factor Index of Social Status. Unpublished Working Paper, Yale University, New Haven, CT.
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, 17941803.
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.
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, 235245.
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.
Fischl, B (2012) Freesurfer. NeuroImage 62, 774781.
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, 341355.
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, 154157.
Friedman, L and Glover, GH (2006) Report on a multicenter fMRI quality assurance protocol. Journal of Magnetic Resonance Imaging 23, 827839.
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, 471481.
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, 3954.
Greenspan, KS, Arakelian, CR and van Erp, TGM (2016) Heritability of hippocampal formation sub-region volumes. Journal of Neurology and Neuroscience 7, 17.
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, 10531061.
Hagihara, H, Takao, K, Walton, NM, Matsumoto, M and Miyakawa, T (2013) Immature dentate gyrus: an endophenotype of neuropsychiatric disorders. Neural Plasticity 2013, 318596.
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, 11291138.
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.
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, 581588.
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, 217226.
Hegyi, H (2017) Connecting myelin-related and synaptic dysfunction in schizophrenia with SNP-rich gene expression hubs. Scientific Reports 7, 45494.
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, 13611370.
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, 142152.
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, 699705.
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, 429438.
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, 766778.
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.
Kay, SR, Opler, LA and Lindenmayer, J-P (1989) The positive and negative syndrome scale (PANSS): rationale and standardisation. British Journal of Psychiatry 155, 5965.
Kubicki, M, McCarley, RW and Shenton, ME (2005) Evidence for white matter abnormalities in schizophrenia. Current Opinion in Psychiatry 18, 121134.
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, 769777.
McInnes, LA and Lauriat, TL (2006) RNA metabolism and dysmyelination in schizophrenia. Neuroscience and Biobehavioral Reviews 30, 551561.
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, 156166.
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.
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, 14601466.
Oldfield, RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97113.
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, 12811292.
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, 5459.
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, 559575.
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, 17061718.
Risch, N and Merikangas, K (1996) The future of genetic studies of complex human diseases. Science 273, 15161517.
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, 15.
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, 395407.
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, 8491.
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, 938946.
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, 8295.
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, 585601.
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, 5966.
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, 1016.
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, 826834.
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.
Tamminga, CA, Stan, AD and Wagner, AD (2010) The hippocampal formation in schizophrenia. The American Journal of Psychiatry 167, 11781193.
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, 927935.
Uttl, B (2002) North American Adult Reading Test: age norms, reliability, and validity. Journal of Clinical and Experimental Neuropsychology 24, 11231137.
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, 235243.
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, 549557.
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.
Watanabe, K, Taskesen, E, van Bochoven, A and Posthuma, D (2017) Functional mapping and annotation of genetic associations with FUMA. Nature Communications 8, 111.
Wheeler, DW, White, CM, Rees, CL, Komendantov, AO, Hamilton, DJ and Ascoli, GA (2015) a knowledge base of neuron types in the rodent hippocampus. eLife 4, 128.
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, 125137.
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.
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, 510517.
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, 385398.
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, 159164.
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, 1556515576.


Type Description Title
Supplementary materials

Nakahara et al. supplementary material
Nakahara et al. supplementary material 1

 Word (127 KB)
127 KB


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed