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Deficits in Small Interneurons in Prefrontal and Cingulate Cortices of Schizophrenic and Schizoaffective Patients
Abstract
A recent report suggested that neurons in the prefrontal, anterior cingulate, and primary motor cortex of the brains of schizophrenic subjects may be less dense than those in the brains of nonschizophrenic subjects. We have determined whether pyramidal neurons and/or interneurons are preferentially reduced in schizophrenic subjects. Twelve control subjects and 18 schizophrenic subjects were studied in a blind, quantitative analysis of the density of pyramidal cells, interneurons, and glial cells in each of the six layers of the anterior cingulate and prefrontal cortex. The results showed that numbers of small neurons (interneurons) were reduced in most layers of the cingulate cortex in schizophrenic subjects compared with nonschizophrenic subjects, with the differences being greatest in layer II. In the prefrontal area, interneuronal density was also lower in layer II and, to a lesser extent, in layer I in schizophrenic subjects compared with control subjects. In most cases, the differences were similar, although more significant, in schizophrenic subjects who had had superimposed mood disturbances than in schizophrenic subjects who had not had such comorbidity. Numbers of pyramidal neurons generally were not different between control and schizophrenic subjects, except in layer V of the prefrontal area, where schizophrenic subjects showed higher densities of these neurons. Glial numbers did not differ between the control and schizophrenic subjects, suggesting that a neurodegenerative process did not cause the reduced interneuronal density observed. Using multiple regression analysis and analysis of covariance, decreases in the density of layer II interneurons could not be adequately explained by the effects of various confounding variables, such as age, postmortem interval, duration of specimen fixation, or administration of neuroleptic agents.(ABSTRACT TRUNCATED AT 250 WORDS)
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Citations
Cites
Prenatal developmental disturbances in the limbic allocortex in schizophrenics
Jakob, H., & Beckmann, H. (1986) · Journal of Neural Transmission · doi:10.1007/bf01249090 · Cited by 875
Cited by
Neurobiology of emotion perception II: implications for major psychiatric disorders
Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00171-9 · Cited by 1,736
Glutamate receptor dysfunction and schizophrenia
Olney, J. W. (1995) · Archives of General Psychiatry · doi:10.1001/archpsyc.1995.03950240016004 · Cited by 1,685
The neuropathology of schizophrenia
Harrison, P. J. (1999) · Brain · doi:10.1093/brain/122.4.593 · Cited by 1,677
Laruelle, M., Abi-Dargham, A., van Dyck, C. H., Gil, R., D'Souza, C. D., Erdos, J., McCance, E., Rosenblatt, W., Fingado, C., Zoghbi, S. S., et al. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.17.9235 · Cited by 1,291
Interneuron dysfunction in psychiatric disorders
Marín, O. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3155 · Cited by 1,190
GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder
Benes, F. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00225-1 · Cited by 1,082
Self-citationLisman, J. E., Coyle, J. T., Green, R. W., Javitt, D. C., Benes, F. M., Heckers, S., & Grace, A. A. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.02.005 · Cited by 1,010
Self-citationAkbarian, S. (1995) · Archives of General Psychiatry · doi:10.1001/archpsyc.1995.03950160008002 · Cited by 1,002
The reduced neuropil hypothesis: a circuit based model of schizophrenia
Selemon, L. D., & Goldman-Rakic, P. S. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00281-9 · Cited by 909
Glutamate and Schizophrenia: Beyond the Dopamine Hypothesis
Coyle, J. T. (2006) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-006-9062-8 · Cited by 917
The Computational Anatomy of Psychosis
Adams, R. A., Stephan, K. E., Brown, H. R., Frith, C. D., & Friston, K. J. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00047 · Cited by 850
“Others have found losses of interneurons in layer 2 in both prefrontal and cingulate cortex (Benes et al., 1991) and smaller dendritic fields of prefrontal layer 5 pyramidal cells (Black et al., 2004).”
BackgroundPrefrontal–hippocampal interactions in episodic memory
Eichenbaum, H. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.74 · Cited by 870
Cotter, D., Mackay, D., Landau, S., Kerwin, R., & Everall, I. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.6.545 · Cited by 766
Benes, F. M. (1994) · Archives of General Psychiatry · doi:10.1001/archpsyc.1994.03950060041004 · Cited by 744
Self-citationNeuroinflammation and psychiatric illness
Najjar, S., Pearlman, D. M., Alper, K., Najjar, A., & Devinsky, O. (2013) · Journal of Neuroinflammation · doi:10.1186/1742-2094-10-43 · Cited by 733
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
Schizophrenia, sensory gating, and nicotinic receptors
Adler, L. E., Olincy, A., Waldo, M., Harris, J. G., Griffith, J., Stevens, K., Flach, K., Nagamoto, H., Bickford, P., Leonard, S., et al. (1998) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033320 · Cited by 690
Freedman, R., Hall, M., Adler, L. E., & Leonard, S. (1995) · Biological Psychiatry · doi:10.1016/0006-3223(94)00252-x · Cited by 678
Functional and Anatomical Aspects of Prefrontal Pathology in Schizophrenia
Goldman-Rakic, P. S., & Selemon, L. D. (1997) · Schizophrenia Bulletin · doi:10.1093/schbul/23.3.437 · Cited by 668
Gamma frequency-range abnormalities to auditory stimulation in schizophrenia
Kwon, J. S., O'Donnell, B. F., Wallenstein, G. V., Greene, R. W., Hirayasu, Y., Nestor, P. G., Hasselmo, M. E., Potts, G. F., Shenton, M. E., & McCarley, R. W. (1999) · Archives of General Psychiatry · doi:10.1001/archpsyc.56.11.1001 · Cited by 654
Cotter, D. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.4.386 · Cited by 634
Schizophrenia susceptibility associated with interstitial deletions of chromosome 22q11.
Karayiorgou, M., Morris, M. A., Morrow, B., Shprintzen, R. J., Goldberg, R., Borrow, J., Gos, A., Nestadt, G., Wolyniec, P. S., & Lasseter, V. K. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.17.7612 · Cited by 628
Rajkowska, G., Selemon, L. D., & Goldman-Rakic, P. S. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.3.215 · Cited by 537
Krystal, J. H., D'Souza, D. C., Mathalon, D., Perry, E., Belger, A., & Hoffman, R. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1582-z · Cited by 530
Emerging principles of altered neural circuitry in schizophrenia
Benes, F. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00041-7 · Cited by 513
Self-citationGABAergic interneuron origin of schizophrenia pathophysiology
Nakazawa, K., Zsiros, V., Jiang, Z., Nakao, K., Kolata, S., Zhang, S., & Belforte, J. E. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.022 · Cited by 498
Electron microscopy of oligodendroglia in severe mental illness
Uranova, N., Orlovskaya, D., Vikhreva, O., Zimina, I., Kolomeets, N., Vostrikov, V., & Rachmanova, V. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00528-7 · Cited by 495
Pharmacology and behavioral pharmacology of the mesocortical dopamine system
Tzschentke, T. M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00033-2 · Cited by 481
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
Self-citationGlial cell abnormalities in major psychiatric disorders: the evidence and implications
Cotter, D. R., Pariante, C. M., & Everall, I. P. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00527-5 · Cited by 465
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
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
Woo, T.-U. W., Walsh, J. P., & Benes, F. M. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.7.649 · Cited by 411
Self-citationLewis, D. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(96)00277-1 · Cited by 388
Neural development, cell-cell signaling, and the “two-hit” hypothesis of schizophrenia
Maynard, T. M., Sikich, L., Lieberman, J. A., & LaMantia, A.-S. (2001) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a006887 · Cited by 383
Beasley, C. L., Zhang, Z. J., Patten, I., & Reynolds, G. P. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01360-4 · Cited by 374
Reduced dorsal and orbital prefrontal gray matter volumes in schizophrenia
Gur, R. E., Cowell, P. E., Latshaw, A., Turetsky, B. I., Grossman, R. I., Arnold, S. E., Bilker, W. B., & Gur, R. C. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.8.761 · Cited by 368
Postmortem evidence of cerebral inflammation in schizophrenia: a systematic review
Trépanier, M. O., Hopperton, K. E., Mizrahi, R., Mechawar, N., & Bazinet, R. P. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.90 · Cited by 360
Bayer, T. A., Falkai, P., & Maier, W. (1999) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(99)00039-4 · Cited by 346
Benes, F. M., Vincent, S. L., & Todtenkopf, M. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01084-8 · Cited by 327
Self-citationRosenberg, D. R., & Lewis, D. A. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903580306 · Cited by 319
Mao, X. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.1519 · Cited by 296
Four-Dimensional Migratory Coordinates of GABAergic Interneurons in the Developing Mouse Cortex
Ang, E. S. B. C., Haydar, T. F., Gluncic, V., & Rakic, P. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05805.2003 · Cited by 282
Beasley, C. L., Pennington, K., Behan, A., Wait, R., Dunn, M. J., & Cotter, D. (2006) · PROTEOMICS · doi:10.1002/pmic.200500069 · Cited by 263
Fornito, A., Yucel, M., Dean, B., Wood, S. J., & Pantelis, C. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn025 · Cited by 259
Lewis, D., Volk, D., & Hashimoto, T. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1673-x · Cited by 253
Pathology of Layer V Pyramidal Neurons in the Prefrontal Cortex of Patients With Schizophrenia
Black, J. E., Kodish, I. M., Grossman, A. W., Klintsova, A. Y., Orlovskaya, D., Vostrikov, V., Uranova, N., & Greenough, W. T. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.4.742 · Cited by 250
Regulation of GABAA Receptor Subunit Expression by Pharmacological Agents
Uusi-Oukari, M., & Korpi, E. R. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002063 · Cited by 213
Abdul-Monim, Z., Neill, J. C., & Reynolds, G. P. (2007) · Journal of Psychopharmacology · doi:10.1177/0269881107067097 · Cited by 206
Perrone-Bizzozero, N. I., Sower, A. C., Bird, E. D., Benowitz, L. I., Ivins, K. J., & Neve, R. L. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.14182 · Cited by 206
Purohit, D. P., Perl, D. P., Haroutunian, V., Powchik, P., Davidson, M., & Davis, K. L. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.3.205 · Cited by 185
Castner, S. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(98)00050-5 · Cited by 187
The expression of proapoptosis genes is increased in bipolar disorder, but not in schizophrenia
Benes, F. M., Matzilevich, D., Burke, R. E., & Walsh, J. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001758 · Cited by 183
Self-citationAkbarian, S., Smith, M. A., & Jones, E. G. (1995) · Brain Research · doi:10.1016/0006-8993(95)00922-d · Cited by 183
The role of oligodendrocyte pathology in schizophrenia
Uranova, N. A., Vostrikov, V. M., Vikhreva, O. V., Zimina, I. S., Kolomeets, N. S., & Orlovskaya, D. D. (2007) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145707007626 · Cited by 176
Long-range synchrony of gamma oscillations and auditory hallucination symptoms in schizophrenia
Mulert, C., Kirsch, V., Pascual-Marqui, R., McCarley, R. W., & Spencer, K. M. (2011) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2010.08.004 · Cited by 165
Wang, C. Z., Yang, S. F., Xia, Y., & Johnson, K. M. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301647 · Cited by 161
Neural basis of psychosis-related behaviour in the infection model of schizophrenia
Meyer, U., & Feldon, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.022 · Cited by 158
Populations of hippocampal inhibitory neurons express different levels of cytochrome c
Gulyás, A. I., Buzsáki, G., Freund, T. F., & Hirase, H. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04814.x · Cited by 142
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
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
Tregellas, J. R., Davalos, D. B., Rojas, D. C., Waldo, M. C., Gibson, L., Wylie, K., Du, Y. P., & Freedman, R. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2006.12.033 · Cited by 143
Wang, 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
Fujiwara, H., Namiki, C., Hirao, K., Miyata, J., Shimizu, M., Fukuyama, H., Sawamoto, N., Hayashi, T., & Murai, T. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.05.044 · Cited by 126
Menzies, L., Ooi, C., Kamath, S., Suckling, J., McKenna, P., Fletcher, P., Bullmore, E., & Stephenson, C. (2007) · Archives of General Psychiatry · doi:10.1001/archpsyc.64.2.156 · Cited by 120
Todtenkopf, M. S., Vincent, S. L., & Benes, F. M. (2005) · Schizophrenia Research · doi:10.1016/j.schres.2004.08.018 · Cited by 118
Self-citationAbekawa, T., Ito, K., Nakagawa, S., & Koyama, T. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0729-8 · Cited by 118
Ohrmann, P., Siegmund, A., Suslow, T., Pedersen, A., Spitzberg, K., Kersting, A., Rothermundt, M., Arolt, V., Heindel, W., & Pfleiderer, B. (2007) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2006.07.002 · Cited by 116
The role of cortical inhibition in the pathophysiology and treatment of schizophrenia
Daskalakis, Z. J., Fitzgerald, P. B., & Christensen, B. K. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.09.006 · Cited by 111
Neuron density and serotonin receptor binding in prefrontal cortex in suicide
Underwood, M. D., Kassir, S. A., Bakalian, M. J., Galfalvy, H., Mann, J. J., & Arango, V. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711000691 · Cited by 100
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
Li, Y.-C., Kellendonk, C., Simpson, E. H., Kandel, E. R., & Gao, W.-J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109718108 · Cited by 78
Specificity in inhibitory systems associated with prefrontal pathways to temporal cortex in Primates
Medalla, M., Lera, P., Feinberg, M., & Barbas, H. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm068 · Cited by 69
The Fragile Brain: Stress Vulnerability, Negative Affect and GABAergic Neurocircuits in Psychosis
Taylor, S. F., Grove, T. B., Ellingrod, V. L., & Tso, I. F. (2019) · Schizophrenia Bulletin · doi:10.1093/schbul/sbz046 · Cited by 67
The neuroanatomy of schizophrenia: circuitry and neurotransmitter systems
Fallon, J. H., Opole, I. O., & Potkin, S. G. (2003) · Clinical Neuroscience Research · doi:10.1016/s1566-2772(03)00022-7 · Cited by 53
Glausier, J. R., Kimoto, S., Fish, K. N., & Lewis, D. A. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.05.010 · Cited by 53
Neuroimaging and plasticity in schizophrenia
Meyer-Lindenberg, A., & Tost, H. (2014) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-139014 · Cited by 33
Williams, M. R., Chaudhry, R., Perera, S., Pearce, R. K. B., Hirsch, S. R., Ansorge, O., Thom, M., & Maier, M. (2013) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-012-0325-8 · Cited by 31
Hayashi, Y., Nihonmatsu-Kikuchi, N., Hisanaga, S.-I., Yu, X.-J., & Tatebayashi, Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033019 · Cited by 31
Neuropathology of Schizophrenia
Harrison, P. J., Lewis, D. A., & Kleinman, J. E. (2010) · Schizophrenia · doi:10.1002/9781444327298.ch18 · Cited by 26
Neuron density is decreased in the prefrontal cortex in Williams syndrome
Lew, C. H., Brown, C., Bellugi, U., & Semendeferi, K. (2017) · Autism Research · doi:10.1002/aur.1677 · Cited by 18
Metadata
- Authors
- Benes, F. M.
- Venue
- Archives of General Psychiatry
- Publisher
- American Medical Association (AMA)
- Published
- 1991-11-01
- Volume
- 48
- Issue
- 11
- Pages
- 996
- ISSN
- 0003-990X (ISSN-L)
- OpenAlex
- W2030564379
- Cited by
- 890
- References
- 1
- FWCI
- 16.69
- Type
- journal article
- Language
- en
- Open access
- closed
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