Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calcium-binding proteins
Open accessAbstract
Background Postmortem studies have provided evidence for abnormalities of the gamma-aminobutyric acid (GABA)-ergic system in schizophrenia, including deficits of GABA-containing interneurons. The calcium-binding proteins parvalbumin, calbindin, and calretinin can be used as markers for specific subpopulations of cortical GABAergic interneurons.Methods Following our previous observation of a reduction in the density of parvalbumin- but not calretinin-immunoreactive cells in the prefrontal cortex (Brodmann area 10) in schizophrenia, we have quantified the laminar density of neurons immunoreactive for the calcium-binding proteins parvalbumin, calbindin, and calretinin in a further prefrontal cortical region (Brodmann area 9) in patients with schizophrenia, bipolar disorder, major depression, and in matched control subjects (each group n = 15).Results Initial statistical analysis revealed reductions in the total cortical density of parvalbumin- and calbindin- but not calretinin-immunoreactive neurons in schizophrenia relative to control subjects. Further analysis comparing individual laminar densities between groups indicated that, following correction for multiple comparisons, only a reduction in calbindin-immunoreactive neurons in cortical layer II in the schizophrenic group attained statistical significance.Conclusions These findings suggest that deficits of specific GABAergic neurons, defined by the presence of calcium-binding proteins, are present in schizophrenia. Trends toward similar reductions are observed in bipolar disorder.
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?
Research on parvalbumin cell density in schizophrenia has yielded conflicting results.
“However, studies investigating PV cell density in schizophrenia have provided mixed results (Beasley et al, 2002;Hashimoto et al, 2003;Tooney and Chahl, 2004;Woo et al, 1997).”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Beasley et al, 2002
A power analysis based on prior findings determined how many parvalbumin neurons were sampled.
“Before low magnification imaging, a power analysis of the number of cells needed to detect a difference in PV cell density, based on prior findings (Beasley et al, 2002), was used to determine the total number of PV neurons to sample.”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Beasley et al, 2002
Earlier findings of seemingly reduced parvalbumin cell density probably reflect lower parvalbumin protein amounts.
“Thus, prior reports of apparently lower PV cell density (Beasley et al, 2002) are likely due to lower levels of PV protein”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Beasley et al, 2002
At low magnification, layer 3 parvalbumin cell density was 11.7% lower in schizophrenia subjects than in comparison subjects (2695 vs 3051 cells per mm3).
“Under low magnification, the mean (± SD) density of layer 3 PV cells in schizophrenia subjects (2695 ±527 cells per mm 3 ) was 11.7% lower (F 1,27 = 7.54, P = 0.011; Figure 2a) compared with that in comparison subjects (3051 ± 416 cells per mm 3 ), a decrement similar to a previous study (Beasley et al, 2002).”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Beasley et al, 2002
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
Hsu, S. M., Raine, L., & Fanger, H. (1981) · Journal of Histochemistry & Cytochemistry · doi:10.1177/29.4.6166661 · Cited by 14,248 · see citing works
Calbindin D-28k and parvalbumin in the rat nervous system
Celio, M. R. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90091-h · Cited by 2,086 · see citing works
Guidotti, A., Auta, J., Davis, J. M., Gerevini, V. D. G., Dwivedi, Y., Grayson, D. R., Impagnatiello, F., Pandey, G. N., Pesold, C., Sharma, R. P., et al. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.11.1061 · Cited by 1,203 · see citing works
Akbarian, S. (1995) · Archives of General Psychiatry · doi:10.1001/archpsyc.1995.03950160008002 · Cited by 1,002 · see citing works
Benes, F. M. (1991) · Archives of General Psychiatry · doi:10.1001/archpsyc.1991.01810350036005 · Cited by 894 · see citing works
Somogyi, P., Hodgson, A., Smith, A. D., Nunzi, M. G., Gorio, A., & Wu, J. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-10-02590.1984 · Cited by 731 · see citing works
Volk, D. W., Austin, M. C., Pierri, J. N., Sampson, A. R., & Lewis, D. A. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.3.237 · Cited by 697 · see citing works
The Stanley Foundation brain collection and Neuropathology Consortium
Torrey, Ε. F., Webster, M. J., Knable, M. B., Johnston, N., & Yolken, R. H. (2000) · Schizophrenia Research · doi:10.1016/s0920-9964(99)00192-9 · Cited by 533 · 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
Self-citationParvalbumin-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
Self-citationA subclass of prefrontal γ-aminobutyric acid axon terminals are selectively altered in schizophrenia
Woo, T.-U. W., Whitehead, R. E., Melchitzky, D. S., & Lewis, D. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5341 · Cited by 410 · see citing works
Rajkowska, G., & Goldman, P. S. (1995) · Cerebral Cortex · doi:10.1093/cercor/5.4.307 · Cited by 392 · see citing works
Immunocytochemical localization of calretinin in the forebrain of the rat
Jacobowitz, D. M., & Winsky, L. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903040205 · Cited by 384 · see citing works
Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex.
DeFelipe, J., Hendry, S. H. C., & Jones, E. G. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.6.2093 · Cited by 338 · see citing works
Benes, F. M., Vincent, S. L., Marie, A. S., & Khan, Y. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00328-4 · Cited by 274 · see citing works
Chana, G., Landau, S., Beasley, C. L., Everall, I., & Cotter, D. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00114-8 · Cited by 245 · see citing works
Self-citationTwo-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
Lewis, D. A., & Lund, J. S. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902930406 · Cited by 220 · see citing works
Regional Brain Concentrations of Neuropeptides in Huntington's Chorea and Schizophrenia
Nemeroff, C. B., Youngblood, W. W., Manberg, P. J., Prange, A. J., & Kizer, J. S. (1983) · Science · doi:10.1126/science.6136092 · Cited by 219 · see citing works
Cotter, D., Landau, S., Beasley, C. L., Stevenson, R. N., Chana, G., MacMillan, L., & Everall, I. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01243-4 · Cited by 211 · see citing works
Self-citationSchizophrenia and the parvalbumin-containing class of cortical local circuit neurons
Woo, T., Miller, J. L., & Lewis, D. A. (1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.7.1013 · Cited by 191 · see citing works
Dános, P. (1998) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(97)00071-1 · Cited by 189 · 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
Heterogeneity of GABAergic cells in cat visual cortex
Demeulemeester, H. G., Vandesande, F., Orban, G. A., Brandon, C. J., & Vanderhaeghen, J. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-03-00988.1988 · Cited by 164 · see citing works
[3H]Muscimol binding sites increased in autopsied brains of chronic schizophrenics
Hanada, S., Mita, T., Nishino, N., & Tanaka, C. (1987) · Life Sciences · doi:10.1016/0024-3205(87)90341-9 · Cited by 140 · see citing works
GABAergic neuronal subtypes in the human frontal cortex — development and deficits in schizophrenia
Reynolds, G. P., & Beasley, C. L. (2001) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(01)00113-2 · Cited by 138 · see citing works
Self-citationBenes, F. M., Todtenkopf, M. S., Logiotatos, P., & Williams, M. (2000) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(00)00105-8 · Cited by 109 · see citing works
Neuropeptide deficits in schizophrenia vs. Alzheimer's disease cerebral cortex.
Gabriel, S., Davidson, M., Haroutunian, V., Powchik, P., Bierer, L., Purohit, D., Perl, D., & Davis, K. (1996) · Biological Psychiatry · doi:10.1016/0006-3223(95)00066-6 · Cited by 88 · see citing works
DeFelipe, J., & Jones, E. G. (1991) · Brain Research · doi:10.1016/0006-8993(91)91184-3 · Cited by 82 · see citing works
Sze, P. Y. (1979) · Advances in experimental medicine and biology · doi:10.1007/978-1-4899-5199-1_4 · Cited by 77 · see citing works
Abnormal cholecystokinin mRNA levels in entorhinal cortex of schizophrenics
Bachus, S. E., Hyde, T. M., Herman, M. M., Egan, M. F., & Kleinman, J. E. (1997) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(96)00041-6 · Cited by 74 · see citing works
Kalus, P., Senitz, D., & Beckmann, H. (1997) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(97)00020-6 · Cited by 67 · see citing works
Carder, R. K., Leclerc, S. S., & Hendry, S. H. C. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.2.271 · Cited by 57 · see citing works
Evers, P., & Uylings, H. B. M. (1994) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(94)90208-9 · Cited by 54 · see citing works
Cholecystokinin messenger RNA deficit in frontal and temporal cerebral cortex in schizophrenia
Virgo, L., Humphries, C., Mortimer, A. M., Barnes, T. R. E., Hirsch, S. R., & de Belleroche, J. (1995) · Biological Psychiatry · doi:10.1016/0006-3223(94)00206-i · Cited by 51 · see citing works
Kamphuis, W., Huisman, E., Wadman, W. J., & Lopes, F. H. D. S. (1989) · Experimental Brain Research · doi:10.1007/bf00248871 · Cited by 47 · see citing works
Akil, M., & Lewis, D. A. (1992) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(92)90084-r · Cited by 28 · see citing works
Two-dimensional versus three-dimensional cell counting
Selemon, L. D., & Rajkowska, G. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01323-9 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
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
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
Hippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · see citing works
Animal models of schizophrenia
Jones, C., Watson, D., & Fone, K. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01386.x · Cited by 771 · see citing works
Ketamine-Induced Loss of Phenotype of Fast-Spiking Interneurons Is Mediated by NADPH-Oxidase
Behrens, M. M., Ali, S. S., Dao, D. N., Lucero, J., Shekhtman, G., Quick, K. L., & Dugan, L. L. (2007) · Science · doi:10.1126/science.1148045 · Cited by 585 · see citing works
González‐Burgos, G., & Lewis, D. A. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn070 · Cited by 568 · see citing works
Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia
Weickert, C. S., Hyde, T. M., Lipska, B. K., Herman, M. M., Weinberger, D. R., & Kleinman, J. E. (2003) · Molecular Psychiatry · doi:10.1038/sj.mp.4001308 · Cited by 533 · see citing works
Neill, J. C., Barnes, S. A., Cook, S., Grayson, B., Idris, N. F., McLean, S. L., Snigdha, S., Rajagopal, L., & Harte, M. (2010) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2010.07.004 · Cited by 525 · see citing works
Rajkowska, G., O'Dwyer, G., Teleki, Z., Stockmeier, C. A., & Miguel-Hidalgo, J. J. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301234 · Cited by 430 · 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
Cortical GABAergic Dysfunction in Stress and Depression: New Insights for Therapeutic Interventions
Fogaça, M. V., & Duman, R. S. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00087 · Cited by 396 · see citing works
Knable, M. B., Barci, B. M., Webster, M. J., Meador‐Woodruff, J. H., & Torrey, Ε. F. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001471 · Cited by 407 · see citing works
Hashimoto, T., Bergen, S. E., Nguyen, Q. L., Xu, B., Monteggia, L. M., Pierri, J. N., Sun, Z., Sampson, A. R., & Lewis, D. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4035-04.2005 · Cited by 384 · 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
Akbarian, S., & Huang, H. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.04.001 · Cited by 362 · see citing works
Altar, C. A., Jurata, L. W., Charles, V., Lemire, A., Liu, P., Bukhman, Y., Young, T. A., Bullard, J., Yokoe, H., Webster, M. J., et al. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.03.031 · Cited by 318 · see citing works
Alterations in cortical interneurons and cognitive function in schizophrenia
Dienel, S. J., & Lewis, D. A. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.06.020 · Cited by 267 · see citing works
Lewis, D., Volk, D., & Hashimoto, T. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1673-x · Cited by 253 · see citing works
Executive Function, Neural Circuitry, and Genetic Mechanisms in Schizophrenia
Eisenberg, D., & Berman, K. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.111 · Cited by 250 · see citing works
Enwright, J. F., Sanapala, S., Foglio, A., Berry, R., Fish, K. N., & Lewis, D. A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.24 · Cited by 223 · see citing works
Cohen, S. M., Tsien, R. W., GOFF, D. C., & Halassa, M. M. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2014.12.026 · Cited by 233 · see citing works
Cabungcal, J.-H., Steullet, P., Kraftsik, R., Cuenod, M., & Do, K. Q. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.09.020 · Cited by 232 · see citing works
Prepulse inhibition and genetic mouse models of schizophrenia
Powell, S. B., Zhou, X., & Geyer, M. A. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.04.021 · Cited by 218 · see citing works
GABA-related transcripts in the dorsolateral prefrontal cortex in mood disorders
Sibille, E., Morris, H. M., Kota, R. S., & Lewis, D. A. (2011) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145710001616 · Cited by 217 · see citing works
Inhibitory control of the excitatory/inhibitory balance in psychiatric disorders
Selten, M. M., van Bokhoven, H., & Kasri, N. N. (2018) · F1000Research · doi:10.12688/f1000research.12155.1 · Cited by 208 · see citing works
Neurodevelopmental effects of insulin-like growth factor signaling
OʼKusky, J. R., & Ye, P. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.06.002 · Cited by 210 · see citing works
Abdul-Monim, Z., Neill, J. C., & Reynolds, G. P. (2007) · Journal of Psychopharmacology · doi:10.1177/0269881107067097 · Cited by 206 · see citing works
Self-citationKeilhoff, G., Becker, A., Grecksch, G., Wolf, G. L., & Bernstein, H. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.03.039 · Cited by 200 · see citing works
Reductions in neurotrophin receptor mRNAs in the prefrontal cortex of patients with schizophrenia
Weickert, C. S., Ligons, D. L., Romanczyk, T. B., Ungaro, G., Hyde, T. M., Herman, M. M., Weinberger, D. R., & Kleinman, J. E. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001678 · Cited by 199 · see citing works
Reduced somatostatin in subgenual anterior cingulate cortex in major depression
Tripp, A., Kota, R. S., Lewis, D. A., & Sibille, E. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.01.014 · Cited by 190 · see citing works
Hwang, Y., Kim, J., Shin, J.-Y., Kim, J.-I., Seo, J.-S., Webster, M. J., Lee, D., & Kim, S. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.94 · Cited by 189 · see citing works
Eastwood, S. L., & Harrison, P. J. (2004) · Schizophrenia Research · doi:10.1016/j.schres.2004.05.010 · Cited by 187 · see citing works
Oxidative stress, prefrontal cortex hypomyelination and cognitive symptoms in schizophrenia
Maas, D. A., Vallès, A., & Martens, G. J. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.138 · Cited by 181 · see citing works
GABAergic Mechanisms in Schizophrenia: Linking Postmortem and In Vivo Studies
de Jonge, J. C., Vinkers, C. H., Pol, H. E. H., & Marsman, A. (2017) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2017.00118 · Cited by 185 · see citing works
Glutamatergic Synaptic Dysregulation in Schizophrenia: Therapeutic Implications
Coyle, J. T., Basu, A., Benneyworth, M., Balu, D., & Konopaske, G. (2012) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-25758-2_10 · Cited by 180 · see citing works
Immune System Disturbances in Schizophrenia
Horváth, S., & Mirnics, K. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.06.010 · Cited by 177 · see citing works
Steullet, P., Cabungcal, J.-H., Bukhari, S. A., Ardelt, M., Pantazopoulos, H., Hamati, F., Salt, T. E., Cuénod, M., Kim, Q., & Berretta, S. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.230 · Cited by 170 · see citing works
The mood stabilizer valproic acid stimulates GABA neurogenesis from rat forebrain stem cells
Laeng, P., Pitts, R. L., Lemire, A. L., Drabik, C. E., Weiner, A., Tang, H., Thyagarajan, R., Mallon, B. S., & Altar, C. A. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02725.x · Cited by 169 · see citing works
Lighting the chandelier: new vistas for axo-axonic cells
Howard, A., Tamas, G., & Soltesz, I. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.04.004 · Cited by 167 · see citing works
Powell, S. B., Sejnowski, T. J., & Behrens, M. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.049 · Cited by 164 · see citing works
Glausier, J. R., Fish, K. N., & Lewis, D. A. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.152 · Cited by 147 · see citing works
Single-cell multi-cohort dissection of the schizophrenia transcriptome
Ruzicka, W. B., Mohammadi, S., Fullard, J. F., Dávila-Velderrain, J., Subburaju, S., Tso, D. R., Hourihan, M., Jiang, S., Lee, H.-C., Bendl, J. M., et al. (2024) · Science · doi:10.1126/science.adg5136 · Cited by 155 · see citing works
Modelling prefrontal cortex deficits in schizophrenia: implications for treatment
Pratt, J. A., Winchester, C. L., Egerton, A., Cochran, S., & Morris, B. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.24 · Cited by 153 · see citing works
Pre-frontal parvalbumin interneurons in schizophrenia: a meta-analysis of post-mortem studies
Kaar, S. J., Angelescu, I., Marques, T. R., & Howes, O. D. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02080-2 · Cited by 146 · see citing works
Crowley, T., Cryan, J. F., Downer, E. J., & O’Leary, O. F. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.02.001 · Cited by 150 · see citing works
Reynolds, G. P., Abdul-Monim, Z., Neill, J. C., & Zhang, Z. (2004) · Neurotoxicity Research · doi:10.1007/bf03033297 · Cited by 150 · see citing works
Self-citationPain-related deactivation of medial prefrontal cortical neurons involves mGluR1 and GABA A receptors
Ji, G., & Neugebauer, V. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00461.2011 · Cited by 150 · see citing works
Gigante, A. D., Young, L. T., Yatham, L. N., Andreazza, A. C., Nery, F. G., Grinberg, L. T., Heinsen, H., & Lafer, B. (2010) · The International Journal of Neuropsychopharmacology · doi:10.1017/s146114571000146x · Cited by 143 · see citing works
Harte, M., Powell, S. B., Swerdlow, N. R., Geyer, M. A., & Reynolds, G. P. (2007) · Journal of Neural Transmission · doi:10.1007/s00702-007-0627-6 · Cited by 146 · see citing works
Self-citationSavitz, J. B., Price, J. L., & Drevets, W. C. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.02.008 · Cited by 145 · see citing works
Pehrson, A. L., & Sánchez, C. (2015) · Drug Design Development and Therapy · doi:10.2147/dddt.s62912 · Cited by 143 · see citing works
Tseng, K. Y., Lewis, B. L., Hashimoto, T., Sesack, S. R., Kloc, M., Lewis, D. A., & O'Donnell, P. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4166-08.2008 · Cited by 144 · see citing works
Haldane, M., & Frangou, S. (2004) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2004.05.040 · Cited by 138 · see citing works
Czeh, B., Simon, M., van der Hart, M. G., Schmelting, B., Hesselink, M. B., & Fuchs, E. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300581 · Cited by 136 · see citing works
Abdul-Monim, Z., Reynolds, G. P., & Neill, J. C. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.01.019 · Cited by 136 · see citing works
Self-citationWang, A. Y., Lohmann, K. M., Yang, C. K., Zimmerman, E. I., Pantazopoulos, H., Herring, N., Berretta, S., Heckers, S., & Konradi, C. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0881-4 · Cited by 135 · see citing works
Banasr, M., Lepack, A., Fee, C., Duric, V., Maldonado-Aviles, J., DiLeone, R., Sibille, E., Duman, R. S., & Sanacora, G. (2017) · Chronic Stress · doi:10.1177/2470547017720459 · Cited by 135 · see citing works
Jaaro-Peled, H., Ayhan, Y., Pletnikov, M. V., & Sawa, A. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp133 · Cited by 134 · see citing works
Calretinin expression in the mammalian neocortex: a review
Barinka, F., & Druga, R. (2010) · Physiological Research · doi:10.33549/physiolres.931930 · Cited by 128 · see citing works
Penschuck, S., Flagstad, P., Didriksen, M., Leist, M., & Michael-Titus, A. T. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04536.x · Cited by 127 · see citing works
Gomes, F. V., Rincón‐Cortés, M., & Grace, A. A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.030 · Cited by 128 · see citing works
GABA abnormalities in schizophrenia: A methodological review of in vivo studies
Taylor, S. F., & Tso, I. F. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.10.011 · Cited by 125 · see citing works
Immature Dentate Gyrus: An Endophenotype of Neuropsychiatric Disorders
Hagihara, H., Takao, K., Walton, N. M., Matsumoto, M., & Miyakawa, T. (2013) · Neural Plasticity · doi:10.1155/2013/318596 · Cited by 123 · see citing works
Yang, Y., Fung, S. J., Rothwell, A. R., Si, T., & Weickert, C. S. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.08.020 · Cited by 123 · see citing works
Sakai, T., Oshima, A., Nozaki, Y., Ida, I., Haga, C., Akiyama, H., Nakazato, Y., & Mikuni, M. (2008) · Neuropathology · doi:10.1111/j.1440-1789.2007.00867.x · Cited by 118 · see citing works
Abekawa, T., Ito, K., Nakagawa, S., & Koyama, T. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0729-8 · Cited by 118 · see citing works
Stedehouder, J., & Kushner, S. A. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.147 · Cited by 113 · see citing works
Toker, L., Mancarci, B. O., Tripathy, S. J., & Pavlidis, P. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.07.010 · Cited by 113 · see citing works
Altered gene expression in the dorsolateral prefrontal cortex of individuals with schizophrenia
Guillozet-Bongaarts, A. L., Hyde, T. M., Dalley, R. A., Hawrylycz, M., Henry, A. M., Hof, P. R., Hohmann, J. G., Jones, A. R., Kuan, C. L., Royall, J. J., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.30 · Cited by 114 · see citing works
Bertram, I., Bernstein, H., Lendeckel, U., Bukowska, A., Dobrowolny, H., Keilhoff, G., Kanakis, D. N., Mawrin, C., Bielau, H., Falkai, P., et al. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1397.080 · Cited by 114 · see citing works
de Almeida, J., & Mengod, G. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04768.x · Cited by 109 · see citing works
Le-Niculescu, H., McFarland, M. J., Ogden, C. A., Balaraman, Y., Patel, S. D., Tan, J., Rodd, Z. A., Paulus, M. P., Geyer, M. A., Edenberg, H. J., et al. (2008) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30707 · Cited by 108 · see citing works
Diurnal rhythms in gene expression in the prefrontal cortex in schizophrenia
Seney, M. L., Cahill, K., Enwright, J. F., Logan, R. W., Huo, Z., Zong, W., Tseng, G., & McClung, C. A. (2019) · Nature Communications · doi:10.1038/s41467-019-11335-1 · Cited by 108 · see citing works
Mechanisms of neurodegeneration in mucopolysaccharidoses II and IIIB: analysis of human brain tissue
Hamano, K., Hayashi, M., Shioda, K., Fukatsu, R., & Mizutani, S. (2007) · Acta Neuropathologica · doi:10.1007/s00401-007-0325-3 · Cited by 106 · see citing works
Pezze, M. A., McGarrity, S., Mason, R., Fone, K. C. F., & Bast, T. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3450-13.2014 · Cited by 106 · see citing works
Deciphering the Disease Process of Schizophrenia: The Contribution of Cortical Gaba Neurons
Lewis, D. A., & Hashimoto, T. (2007) · International review of neurobiology · doi:10.1016/s0074-7742(06)78004-7 · Cited by 105 · see citing works
Altered fatty acid concentrations in prefrontal cortex of schizophrenic patients
Taha, A. Y., Cheon, Y., Ma, K., Rapoport, S. I., & Rao, J. S. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.01.016 · Cited by 105 · see citing works
Cxcr4 regulation of interneuron migration is disrupted in 22q11.2 deletion syndrome
Meechan, D. W., Tucker, E. S., Maynard, T. M., & LaMantia, A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211507109 · Cited by 101 · see citing works
Oh, D. H., Son, H., Hwang, S., & Kim, S. H. (2012) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2011.09.001 · Cited by 103 · see citing works
Molecular neurobiology of bipolar disorder: a disease of ‘mood-stabilizing neurons’?
Kato, T. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.07.007 · Cited by 102 · see citing works
Rao, J. S., Kellom, M., Reese, E. A., Rapoport, S. I., & Kim, H. (2011) · Journal of Affective Disorders · doi:10.1016/j.jad.2011.08.017 · Cited by 101 · see citing works
RetractedLosing your inhibition: Linking cortical GABAergic interneurons to schizophrenia
Inan, M., Petros, T. J., & Anderson, S. A. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.11.013 · Cited by 100 · see citing works
Possible Mechanisms of Neurodegeneration in Schizophrenia
Pérez‐Neri, I., Ramírez‐Bermúdez, J., Montes, S., & Rı́os, C. (2006) · Neurochemical Research · doi:10.1007/s11064-006-9162-3 · Cited by 100 · see citing works
Cohen, S. M., Ma, H., Kuchibhotla, K. V., Watson, B. O., Buzsáki, G., Froemke, R. C., & Tsien, R. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.001 · Cited by 100 · see citing works
Medalla, M., & Barbas, H. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1773-10.2010 · Cited by 102 · see citing works
Meechan, D. W., Maynard, T. M., Tucker, E. S., Fernandez, A., Karpinski, B. A., Rothblat, L. A., & LaMantia, A. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.03.004 · Cited by 97 · see citing works
Cabungcal, J.-H., Nicolas, D., Kraftsik, R., Cuénod, M., Do, K. Q., & Hornung, J.-P. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.01.003 · Cited by 96 · see citing works
Prenatal stress and inhibitory neuron systems: implications for neuropsychiatric disorders
Fine, R., Zhang, J., & Stevens, H. E. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.35 · Cited by 96 · see citing works
Johnson, A. W., Jaaro-Peled, H., Shahani, N., Sedlak, T. W., Zoubovsky, S., Burruss, D., Emiliani, F., Sawa, A., & Gallagher, M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307925110 · Cited by 96 · see citing works
The Role of the GABAergic System in Diseases of the Central Nervous System
Zhang, W., Xiong, B., Zhang, L.-Q., Huang, X., Yuan, X., Tian, Y., & Tian, X. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.06.037 · Cited by 93 · see citing works
Amitai, N., Kuczenski, R. T., Behrens, M. M., & Markou, A. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.008 · Cited by 90 · see citing works
Dysregulation of GABAergic Neurotransmission in Mood Disorders
Bielau, H., Steiner, J. H., Mawrin, C., Trübner, K., Brisch, R., Meyer-Lotz, G., Brodhun, M., Dobrowolny, H., Baumann, B., Gos, T., et al. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1397.081 · Cited by 90 · see citing works
Dysregulated ErbB4 Splicing in Schizophrenia: Selective Effects on Parvalbumin Expression
Chung, D. W., Volk, D. W., Arion, D., Zhang, Y., Sampson, A. R., & Lewis, D. A. (2016) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2015.15020150 · Cited by 86 · see citing works
Specialized prefrontal “auditory fields”: organization of primate prefrontal-temporal pathways
Medalla, M., & Barbas, H. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00077 · Cited by 86 · see citing works
Zhang, X.-M. (2009) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.017.2009 · Cited by 87 · see citing works
Shah, A., & Lodge, D. J. (2013) · Translational Psychiatry · doi:10.1038/tp.2012.145 · Cited by 87 · see citing works
Models of Neurodevelopmental Abnormalities in Schizophrenia
Powell, S. B. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_57 · Cited by 84 · see citing works
DNA methylation changes in schizophrenia and bipolar disorder
Connor, C., & Akbarian, S. (2008) · Epigenetics · doi:10.4161/epi.3.2.5938 · Cited by 84 · see citing works
Cabungcal, J.-H., Preissmann, D., Delseth, C., Cuénod, M., Kim, Q., & Schenk, F. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.03.001 · Cited by 83 · see citing works
- Authors
- Beasley, C. L., Zhang, Z. J., Patten, I., & Reynolds, G. P.
- Affiliations
- University of Sheffield (GB)
- Corresponding author
- Beasley, Clare L
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2002-10
- Volume
- 52
- Issue
- 7
- Pages
- 708-715
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W1969171865
- Cited by
- 374
- References
- 38
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 16 · 2023: 11 · 2022: 12 · 2021: 11 · 2020: 14 · 2019: 20 · 2018: 14 · 2017: 14 · 2016: 21 · 2015: 23 · 2014: 22 · 2013: 20 · 2012: 19
- FWCI
- 6.40
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (Queen's University Belfast) (submittedVersion)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- schizophrenia, GABAergic interneurons, prefrontal cortex, calcium-binding proteins, parvalbumin, calbindin, calretinin, bipolar disorder, major depressive disorder, Brodmann area 9, Brodmann area 10
- MeSH terms
- Adult, Calcium-Binding Proteins, Cell Count, Female, gamma-Aminobutyric Acid, Humans, Immunohistochemistry, Interneurons, Male, Middle Aged, Parvalbumins, Schizophrenia, Prefrontal Cortex, Calbindins, S100 Calcium Binding Protein G, Calbindin 2
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