Abnormal interneuron development in disrupted-in-schizophrenia-1 L100P mutant mice
Open accessAbstract
Background: Interneuron deficits are one of the most consistent findings in post-mortem studies of schizophrenia patients and are likely important in the cognitive deficits associated with schizophrenia. Disrupted-in-Schizophrenia 1 (DISC1), a strong susceptibility gene for schizophrenia and other mental illnesses, is involved in neurodevelopment, including that of interneurons. However, the mechanism by which DISC1 regulates interneuron development remains unknown. In this study, we analyzed interneuron histology in the Disc1-L100P single point mutation mouse, that was previously shown to have behavioral abnormalities and cortical developmental defects related to schizophrenia. Results: We sought to determine whether a Disc1-L100P point mutation in the mouse would alter interneuron density and location. First, we examined interneuron position in the developing mouse cortex during embryonic days 14–16 as an indicator of interneuron tangential migration, and found striking migration deficits in Disc1-L100P mutants. Further analysis of adult brains revealed that the Disc1-L100P mutants have selective alterations of calbindin- and parvalbumin-expressing interneurons in the cortex and hippocampus, decreased GAD67/PV co-localization and mis-positioned interneurons across the neocortex when compared to wild-type littermates. Conclusion: Our results are consistent with the anomalies seen in post-mortem schizophrenia studies and other Disc1 mutant mouse models. Future research is required to determine the specific mechanisms underlying these cellular deficits. Overall, these findings provide further evidence that DISC1 participates in interneuron development and add to our understanding of how DISC1 variants can affect susceptibility to psychiatric illness.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Mouse models relevant to both schizophrenia and bipolar disorder, including Disc1 and Bdnf models, show abnormal PV-IN function ranging from migration deficits to reduced interneuron number.
“Mouse models relevant for both disorders, including the disrupted in schizophrenia 1 gene (Disc1) [57][58][59][60][61], or brain derived neurotrophic factor (Bdnf) [62], show abnormal PV-IN function ranging from migration deficits to reduction in IN number.”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [57]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
Parvalbumin neurons and gamma rhythms enhance cortical circuit performance
Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K. (2009) · Nature · doi:10.1038/nature07991 · Cited by 2,606 · see citing works
Driving fast-spiking cells induces gamma rhythm and controls sensory responses
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I. (2009) · Nature · doi:10.1038/nature08002 · Cited by 2,603 · see citing works
Cortical inhibitory neurons and schizophrenia
Lewis, D. A., Hashimoto, T., & Volk, D. W. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1648 · Cited by 2,297 · see citing works
Abnormal neural oscillations and synchrony in schizophrenia
Uhlhaas, P. J., & Singer, W. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2774 · Cited by 2,120 · see citing works
Interneuron Migration from Basal Forebrain to Neocortex: Dependence on <i>Dlx</i> Genes
Anderson, S. A., Eisenstat, D. D., Shi, L., & Rubenstein, J. L. R. (1997) · Science · doi:10.1126/science.278.5337.474 · Cited by 1,462 · see citing works
Disruption of two novel genes by a translocation co-segregating with schizophrenia
Millar, J. K. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.9.1415 · Cited by 1,254 · see citing works
Interneuron dysfunction in psychiatric disorders
Marín, O. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3155 · Cited by 1,190 · see citing works
Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia
Lewis, D. A., Curley, A. A., Glausier, J. R., & Volk, D. W. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.10.004 · Cited by 1,071 · see citing works
Akbarian, S. (1995) · Archives of General Psychiatry · doi:10.1001/archpsyc.1995.03950160008002 · Cited by 1,002 · see citing works
The origin and specification of cortical interneurons
Wonders, C. P., & Anderson, S. A. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1954 · Cited by 980 · see citing works
Hashimoto, T., Volk, D. W., Eggan, S. M., Mirnics, K., Pierri, J. N., Sun, Z., Sampson, A. R., & Lewis, D. A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-15-06315.2003 · Cited by 938 · see citing works
Gamma Oscillations Correlate with Working Memory Load in Humans
Howard, M. W. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg084 · Cited by 766 · see citing works
Carlén, M., Meletis, K., Siegle, J. H., Cardin, J. A., Futai, K., Vierling-Claassen, D., Rühlmann, C., Jones, S. R., Deisseroth, K., Sheng, M., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.31 · Cited by 669 · see citing works
The DISC locus in psychiatric illness
Chubb, J. E., Bradshaw, N. J., Soares, D. C., Porteous, D. J., & Millar, J. K. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002106 · Cited by 542 · see citing works
Disrupted-In-Schizophrenia 1 Regulates Integration of Newly Generated Neurons in the Adult Brain
Duan, X., Chang, J. H., Ge, S., Faulkner, R. L., Kim, J. Y., Kitabatake, Y., Liu, X.-B., Yang, C.-H., Jordan, J. D., Ma, D. K., et al. (2007) · Cell · doi:10.1016/j.cell.2007.07.010 · Cited by 538 · see citing works
A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development
Kamiya, A., Kubo, K., Tomoda, T., Takaki, M., Youn, R., Ozeki, Y., Sawamura, N., Park, U., Kudo, C., Okawa, M., et al. (2005) · Nature Cell Biology · doi:10.1038/ncb1328 · Cited by 531 · see citing works
Behavioral phenotypes of Disc1 missense mutations in mice
Clapcote, S. J., Lipina, T. V., Millar, J. K., Mackie, S., Christie, S., Ogawa, F., Lerch, J. P., Trimble, K., Uchiyama, M., Sakuraba, Y., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.04.015 · Cited by 526 · see citing works
Self-citationLodge, D. J., Behrens, M. M., & Grace, A. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5419-08.2009 · Cited by 488 · see citing works
A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives
Benes, F. M., Kwok, E. W., Vincent, S. L., & Todtenkopf, M. S. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00138-3 · Cited by 470 · see citing works
Zhang, Z. J., & Reynolds, G. P. (2002) · Schizophrenia Research · doi:10.1016/s0920-9964(01)00188-8 · Cited by 460 · see citing works
Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1
Flames, N., Long, J. E., Garratt, A. N., Fischer, T. M., Gassmann, M., Birchmeier, C., Lai, C., Rubenstein, J. L. R., & Marı́n, O. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.028 · Cited by 431 · see citing works
Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics
BEASLEY, C., & REYNOLDS, G. (1997) · Schizophrenia Research · doi:10.1016/s0920-9964(96)00122-3 · Cited by 426 · see citing works
Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains
Torrey, E. F., Barci, B. M., Webster, M. J., Bartko, J. J., Meador-Woodruff, J. H., & Knable, M. B. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.10.019 · Cited by 426 · see citing works
Linking neurodevelopmental and synaptic theories of mental illness through DISC1
Brandon, N. J., & Sawa, A. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3120 · Cited by 422 · see citing works
Hikida, T., Jaaro-Peled, H., Seshadri, S., Oishi, K., Hookway, C., Kong, S., Wu, D., Xue, R., Andradé, M., Tankou, S. K., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704774104 · Cited by 417 · see citing works
Fung, S. J., Webster, M. J., Sivagnanasundaram, S., Duncan, C., Elashoff, M., & Weickert, C. S. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2010.09060784 · Cited by 366 · see citing works
Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling
Polleux, F., Whitford, K. L., Dijkhuizen, P. A., Vitalis, T., & Ghosh, A. (2002) · Development · doi:10.1242/dev.129.13.3147 · Cited by 361 · see citing works
Jaaro-Peled, H., Hayashi‐Takagi, A., Seshadri, S., Kamiya, A., Brandon, N. J., & Sawa, A. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.05.007 · Cited by 315 · see citing works
Haenschel, C., Bittner, R. A., Waltz, J., Haertling, F., Wibral, M., Singer, W., Linden, D. E. J., & Rodriguez, E. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1428-09.2009 · Cited by 303 · see citing works
Niwa, M., Kamiya, A., Murai, R., Kubo, K., Gruber, A. J., Tomita, K., Lu, L., Tomisato, S., Jaaro-Peled, H., Seshadri, S., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.019 · Cited by 291 · see citing works
Tóth, K., & Freund, T. F. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90357-8 · Cited by 260 · see citing works
Alterations of cortical GABA neurons and network oscillations in schizophrenia
Gonzalez-Burgos, G., Hashimoto, T., & Lewis, D. A. (2010) · Current Psychiatry Reports · doi:10.1007/s11920-010-0124-8 · Cited by 260 · see citing works
Schizophrenia-Related Neural and Behavioral Phenotypes in Transgenic Mice Expressing TruncatedDisc1
Shen, S., Lang, B., Nakamoto, C., Zhang, F., Pu, J., Kuan, S. L., Chatzi, C. A., He, S., Mackie, I., Brandon, N. J., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3299-08.2008 · Cited by 250 · see citing works
Minzenberg, M. J., Firl, A. J., Yoon, J. H., Gomes, G. C., Reinking, C., & Carter, C. S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.150 · Cited by 247 · see citing works
Dlx transcription factors promote migration through repression of axon and dendrite growth
Cobos, I., Borello, U., & Rubenstein, J. L. R. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.024 · Cited by 246 · see citing works
GABA Neuron Alterations, Cortical Circuit Dysfunction and Cognitive Deficits in Schizophrenia
González‐Burgos, G., Fish, K. N., & Lewis, D. A. (2011) · Neural Plasticity · doi:10.1155/2011/723184 · Cited by 244 · see citing works
Two-dimensional versus three-dimensional cell counting: a practical perspective
Benes, F. M., & LANGE, N. D. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01660-x · Cited by 223 · see citing works
The Cell-Intrinsic Requirement of Sox6 for Cortical Interneuron Development
Batista-Brito, R., Rossignol, E., Hjerling-Leffler, J., Denaxa, M., Wegner, M., Lefebvre, V., Pachnis, V., & Fishell, G. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.005 · Cited by 214 · cited 1× · see citing works
“However, interneuron tangential migration deficits are likely to arise through the simultaneous dysregulation of not just one, but several protein interactions including cytoskeletal proteins [31], dysbindin [2], neurotrophins [36] and transcription factors [37-39].”
BackgroundHippocampal Pathology in Schizophrenia
Heckers, S., & Konradi, C. L. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_43 · Cited by 208 · see citing works
SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development
Azim, E., Jabaudon, D., Fame, R. M., & Macklis, J. D. (2009) · Nature Neuroscience · doi:10.1038/nn.2387 · Cited by 202 · see citing works
DISC1-binding proteins in neural development, signalling and schizophrenia
Bradshaw, N. J., & Porteous, D. J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.12.027 · Cited by 188 · see citing works
DAVISS, S. R., & Lewis, D. A. (1995) · Psychiatry Research · doi:10.1016/0165-1781(95)02720-3 · Cited by 187 · see citing works
The development of hippocampal interneurons in rodents
Danglot, L., Triller, A., & Marty, S. (2006) · Hippocampus · doi:10.1002/hipo.20225 · Cited by 167 · see citing works
Ayhan, Y., Abazyan, B., Nomura, J., Kim, R., Ladenheim, B., Krasnova, I. N., Sawa, A., Margolis, R. L., Cadet, J. L., Mori, S., et al. (2011) · Molecular Psychiatry · doi:10.1038/mp.2009.144 · Cited by 148 · see citing works
The GABAergic system in schizophrenia.
Blum, B. P., & Mann, J. (2002) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145702002894 · Cited by 143 · see citing works
Disc1 Point Mutations in Mice Affect Development of the Cerebral Cortex
Lee, F. H. F., Fadel, M. P., Preston-Maher, K., Cordes, S. P., Clapcote, S. J., Price, D. J., Roder, J., & Wong, A. H. C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4219-10.2011 · Cited by 123 · see citing works
Self-citationGolgi Atlas of the Postnatal Mouse Brain
Valverde, F. (1998) · Springer eBooks · doi:10.1007/978-3-7091-6501-0 · Cited by 90 · see citing works
Disrupted-in-Schizophrenia 1 (DISC1) Is Necessary for the Correct Migration of Cortical Interneurons
Steinecke, A., Gampe, C., Valkova, C., Kaether, C., & Bolz, J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5036-11.2012 · Cited by 69 · see citing works
Li, H., Chou, S., Hamasaki, T., Pérez‐García, C. G., & O’Leary, D. D. M. (2012) · Neural Development · doi:10.1186/1749-8104-7-10 · Cited by 57 · see citing works
Control of tangential/non-radial migration of neurons in the developing cerebral cortex
Nakajima, K. (2007) · Neurochemistry International · doi:10.1016/j.neuint.2007.05.006 · Cited by 56 · see citing works
Ušaj, M., Torkar, D., Kandušer, M., & Damijan Miklavčič, A. (2010) · Journal of Microscopy · doi:10.1111/j.1365-2818.2010.03441.x · Cited by 38 · see citing works
Immunohistochemical analysis of Disc1 expression in the developing and adult hippocampus
Meyer, K. D., & Morris, J. A. (2008) · Gene Expression Patterns · doi:10.1016/j.gep.2008.06.005 · Cited by 35 · see citing works
Evidence Linking DISC1 Gene to Mental Illness Builds
Marx, J. L. (2007) · Science · doi:10.1126/science.318.5853.1062 · Cited by 8 · see citing works
Place Cell Activity in Disc1-L100P Mutant Mice
Mesbah-Oskui, B. L. (2011) · Library and Archives Canada (Government of Canada) · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Gao, R., & Penzes, P. (2015) · Current Molecular Medicine · doi:10.2174/1566524015666150303003028 · Cited by 516 · see citing works
“Likewise, PV+ interneurons in transgenic mice expressing truncated or missense mutated DISC1 are reduced and mislocalized [130, 131].”
BackgroundParvalbumin interneuron vulnerability and brain disorders
Ruden, J. B., Dugan, L. L., & Konradi, C. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-020-0778-9 · Cited by 194 · see citing works
Klune, C. B., Jin, B., & DeNardo, L. A. (2021) · eLife · doi:10.7554/elife.64567 · Cited by 171 · see citing works
GABAergic inhibitory neurons as therapeutic targets for cognitive impairment in schizophrenia
Xu, M., & Wong, A. H. C. (2018) · Acta Pharmacologica Sinica · doi:10.1038/aps.2017.172 · Cited by 159 · see citing works
Self-citationde Bartolomeis, A., Latte, G., Tomasetti, C., & Iasevoli, F. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8534-3 · Cited by 126 · see citing works
Delays in GABAergic interneuron development and behavioral inhibition after prenatal stress
Lussier, S. J., & Stevens, H. E. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22376 · Cited by 89 · see citing works
Volk, D. W., & Lewis, D. A. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu111 · Cited by 86 · see citing works
Neuronal migration abnormalities and its possible implications for schizophrenia
Muraki, K., & Tanigaki, K. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00074 · Cited by 83 · see citing works
Interneuronopathies and their role in early life epilepsies and neurodevelopmental disorders
Katsarou, A., Moshé, S. L., & Galanopoulou, A. S. (2017) · Epilepsia Open · doi:10.1002/epi4.12062 · Cited by 82 · see citing works
Fujihara, K., Miwa, H., Kakizaki, T., Kaneko, R., Mikuni, M., Tanahira, C., Tamamaki, N., & Yanagawa, Y. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.117 · Cited by 81 · see citing works
Tse, M., Piantadosi, P. T., & Floresco, S. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.09.007 · Cited by 73 · see citing works
Seshadri, S., Faust, T. E., Ishizuka, K., Delevich, K. M., Chung, Y., Kim, S.-H., Cowles, M. W., Niwa, M., Jaaro-Peled, H., Tomoda, T., et al. (2015) · Nature Communications · doi:10.1038/ncomms10118 · Cited by 66 · see citing works
Utility and validity of DISC1 mouse models in biological psychiatry
Tomoda, T., Sumitomo, A., Jaaro-Peled, H., & Sawa, A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.12.061 · Cited by 68 · see citing works
Foxp2 regulates neuronal differentiation and neuronal subtype specification
Chiu, Y.-C., Li, M., Liu, Y., Ding, J., Yu, J., & Wang, T. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22166 · Cited by 61 · see citing works
Mouse Genetic Models of Human Brain Disorders
Leung, C., & Jia, Z. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00040 · Cited by 59 · see citing works
Wong, A. H. C., & Josselyn, S. A. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.04.023 · Cited by 55 · see citing works
Self-citationHartung, H., Cichon, N., Feo, V. D., Riemann, S., Schildt, S., Lindemann, C., Mulert, C., Gogos, J. A., & Hanganu‐Opatz, I. L. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw274 · Cited by 47 · see citing works
Kobayashi, M., Nakatani, T., Koda, T., Matsumoto, K., Ozaki, R., Mochida, N., Takao, K., Miyakawa, T., & Matsuoka, I. (2014) · Molecular Brain · doi:10.1186/1756-6606-7-12 · Cited by 46 · see citing works
Different Paths to Core Pathology: The Equifinal Model of the Schizophrenia Syndrome
Green, I. W., & Glausier, J. R. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv136 · Cited by 44 · see citing works
NAKAI, T., Nagai, T., Wang, R., Yamada, S., Kuroda, K., Kaibuchi, K., & Yamada, K. (2014) · Neurochemistry International · doi:10.1016/j.neuint.2014.06.009 · Cited by 41 · see citing works
Santos‐Silva, T., Fabris, D. D. S., de Oliveira, C. L., Guimarães, F. S., & Gomes, F. V. (2023) · Schizophrenia Bulletin · doi:10.1093/schbul/sbad123 · Cited by 42 · see citing works
Schizophrenia, a disease of impaired dynamic metabolic flexibility: A new mechanistic framework
Sarnyai, Z., & Ben‐Shachar, D. (2024) · Psychiatry Research · doi:10.1016/j.psychres.2024.116220 · Cited by 40 · see citing works
Cell migration in the developing rodent olfactory system
Huilgol, D., & Tole, S. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2172-7 · Cited by 30 · see citing works
Su, P., Lai, T. K. Y., Lee, F. H. F., Abela, A. R., Fletcher, P. J., & Liu, F. (2019) · Science Signaling · doi:10.1126/scisignal.aau9122 · Cited by 24 · see citing works
Self-citationDelevich, K. M., Jaaro-Peled, H., Penzo, M. A., Sawa, A., & Li, B. (2020) · eNeuro · doi:10.1523/eneuro.0496-19.2020 · Cited by 25 · see citing works
Full function of exon junction complex factor, Rbm8a, is critical for interneuron development
McSweeney, C., Dong, F., Chen, M. K., Vitale, J., Xu, L., Crowley, N. A., Lüscher, B., Zou, D., & Mao, Y. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-01065-0 · Cited by 22 · see citing works
Neuregulin-1 Regulates Cortical Inhibitory Neuron Dendrite and Synapse Growth through DISC1
Unda, B. K., Kwan, V., & Singh, K. K. (2016) · Neural Plasticity · doi:10.1155/2016/7694385 · Cited by 19 · see citing works
Umeda, K., Iritani, S., Fujishiro, H., Sekiguchi, H., Torii, Y., Habuchi, C., Kuroda, K., Kaibuchi, K., & Ozaki, N. (2016) · Synapse · doi:10.1002/syn.21924 · Cited by 18 · see citing works
Application of animal experimental models in the research of schizophrenia
Wang, P., Li, M., Zhao, A., & Ma, J. (2021) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32863 · Cited by 13 · see citing works
Borkowska, M., Millar, J. K., & Price, D. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0156082 · Cited by 13 · see citing works
Nozari, M., Suzuki, T., Rosa, M. G. P., Yamakawa, K., & Atapour, N. (2016) · Developmental Psychobiology · doi:10.1002/dev.21453 · Cited by 13 · see citing works
Lai, C., Baskaran, R., Tsao, C.-Y., Tuan, L., Siow, P.-F., Palani, M., Lee, L. J., Liu, C., Hwu, H., & Lee, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23169419 · Cited by 9 · see citing works
Mesbah-Oskui, L., Georgiou, J., & Roder, J. (2015) · Schizophrenia · doi:10.1038/npjschz.2015.11 · Cited by 10 · see citing works
Self-citationMorosawa, S., Iritani, S., Fujishiro, H., Sekiguchi, H., Torii, Y., Habuchi, C., Kuroda, K., Kaibuchi, K., & Ozaki, N. (2017) · Neuropeptides · doi:10.1016/j.npep.2016.12.010 · Cited by 10 · see citing works
Deng, D., Jian, C., Lei, L., Zhou, Y., McSweeney, C., Dong, F., Shen, Y., Zou, D., Wang, Y., Wu, Y., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.21381 · Cited by 9 · see citing works
The DISC1 R264Q variant increases affinity for the dopamine D2 receptor and increases GSK3 activity
Su, P., Zhang, H., Wong, A. H. C., & Liu, F. (2020) · Molecular Brain · doi:10.1186/s13041-020-00625-1 · Cited by 8 · see citing works
Self-citationVakalopoulos, C. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00277 · Cited by 7 · see citing works
Auger, M. L., Meccia, J., Galea, L. A. M., & Floresco, S. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1769-z · Cited by 7 · see citing works
What Can We Learn from Animal Models to Study Schizophrenia?
Crunfli, F., Brandão‐Teles, C., Zuccoli, G. S., Filho, A. J. M. C., Vieira, G. M., Silva-Amaral, D., Crippa, J. A. S., Pedrazzi, J. F. C., Macêdo, D. S., Bel, E. A. D., et al. (2022) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-97182-3_2 · Cited by 6 · see citing works
Yang, Z., Xiao, X., Chen, R., Xu, X., Kong, W., & Zhang, T. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.03.011 · Cited by 6 · see citing works
Baskaran, R., Lai, C., Li, W., Tuan, L., Wang, C., Lee, L. J., Liu, C., Hwu, H., & Lee, L. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24813 · Cited by 6 · see citing works
Islam, K. U. S., & Blaess, S. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1403402 · Cited by 5 · see citing works
Shi, S., Chen, T., Su, H., & Zhao, M. (2025) · The Neuroscientist · doi:10.1177/10738584241310156 · Cited by 4 · see citing works
Fingolimod increases parvalbumin-positive neurons in adult mice
Ueno, H., Takahashi, Y., Murakami, S., Wani, K., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2022) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2022.06.005 · Cited by 3 · see citing works
Becerra-Hernández, L. V., Ortiz‐Muñoz, D., Escobar, A. S., González-Acosta, C. A., Buriticá, E., & Martínez-Cerdeño, V. (2026) · Brain Research · doi:10.1016/j.brainres.2025.150141 · Cited by 3 · see citing works
Su, P., Wong, A. H. C., & Liu, F. (2015) · Royal Society of Chemistry eBooks · doi:10.1039/9781782622499-00202 · Cited by 2 · see citing works
Self-citationDelevich, K. M., Jaaro-Peled, H., Penzo, M. A., Sawa, A., & Li, B. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/054759 · Cited by 2 · see citing works
Anderson, Miranda, M., & Qiu, S. (2014)
Lai, T. K. Y. (2019) · TSpace (University of Toronto)
- Authors
- Lee, F. H., Zai, C. C., Cordes, S. P., Roder, J. C., & Wong, A. H.
- Affiliations
- Centre for Addiction and Mental Health (CA)
- Mount Sinai Hospital (CA)
- Corresponding author
- Wong, Albert HC
- Venue
- Molecular Brain
- Published
- 2013-04-30
- Volume
- 6
- Issue
- 1
- Pages
- 20-20
- ISSN
- 1756-6606 (ISSN-L)
- PMC
- PMC3648430
- OpenAlex
- W2121476953
- Cited by
- 49
- References
- 57
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 3 · 2020: 4 · 2019: 3 · 2018: 2 · 2017: 3 · 2016: 10 · 2015: 8 · 2014: 7 · 2013: 1
- FWCI
- 6.13
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Molecular Brain (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- TSpace (University of Toronto) (submittedVersion)
- Funders
- American Foundation for Suicide Prevention
- Eli Lilly and Company
- National Alliance for Research on Schizophrenia and Depression
- Centre for Addiction and Mental Health Foundation
- Canadian Institutes of Health Research
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- DISC1, schizophrenia, interneuron development, tangential migration, parvalbumin interneurons, GAD67, hippocampus, neocortex, cortical development, brain development
- MeSH terms
- Animals, Cell Count, Cell Movement, Embryo, Mammalian, Glutamate Decarboxylase, Hippocampus, Interneurons, Mice, Inbred C57BL, Mice, Neurologic Mutants, Nerve Tissue Proteins, Parvalbumins, Schizophrenia, Point Mutation, Prefrontal Cortex, Neocortex, Mice, Calbindins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
