Expression of Interneuron Markers in the Dorsolateral Prefrontal Cortex of the Developing Human and in Schizophrenia
Abstract
OBJECTIVE: The onset of schizophrenia symptoms in late adolescence implies a neurodevelopmental trajectory for the disease. Indeed, the γ-aminobutyric acid (GABA) inhibitory system shows protracted development, and GABA-ergic deficits are widely replicated in postmortem schizophrenia studies. The authors examined expression of several interneuron markers across postnatal human development and in schizophrenia to assess whether protracted development of certain interneuron subpopulations may be associated with a particular vulnerability in schizophrenia. METHOD: RNA was extracted postmortem from dorsolateral prefrontal cortex of individuals from age 6 weeks to 49 years (N=68) and from a cohort of normal comparison subjects and schizophrenia patients (N=74, 37 pairs). Expression levels of parvalbumin, cholecystokinin, somatostatin, neuropeptide Y, calretinin, calbindin, and vasoactive intestinal peptide were measured by quantitative reverse transcription-polymerase chain reaction. Changes in calretinin protein levels were examined by Western blot. RESULTS: Interneuron marker genes followed one of three general expression profiles: either increasing (parvalbumin, cholecystokinin) or decreasing (somatostatin, calretinin, neuropeptide Y) in expression over postnatal life, with the most dramatic changes seen in the first few years before reaching a plateau; or increasing to peak expression in the toddler years before decreasing (calbindin, vasoactive intestinal peptide). mRNA expression of all genes, with the exception of calbindin (which increased), showed a reduction (8%-31%) in schizophrenia. Somatostatin showed the most dramatic reduction (31%) in schizophrenia. CONCLUSIONS: It appears that a heterogeneous population of interneurons is implicated in schizophrenia. Further studies are needed to determine whether specific interneuron subpopulations are altered or whether common or distinct upstream pathways are responsible for interneuron deficits in schizophrenia.
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Parvalbumin mRNA is reduced in schizophrenia, with the decrease specific to layers 3 and 4.
“lower levels of PV mRNA specifically in layers 3 and 4 (Fung et al, 2010;Hashimoto et al, 2003)”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Fung et al, 2010
In humans, mRNA for GABA receptor subunits and markers of inhibitory cell bodies change substantially across postnatal development, with some specific subunits and markers showing either positive or negative inflections around 10 years of age.
“In humans, mRNA for GABA receptor subunits (Duncan et al., 2010; Fillman et al., 2010) and markers of inhibitory cell bodies (Fung et al., 2010) change substantially across postnatal development, with some specific subunits and markers showing either positive or negative inflections around 10 years of age.”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Fung et al., 2010
GABA receptors in frontal cortex demonstrate peripubertal changes that may influence cortical processing and plasticity.
“GABA receptors in frontal cortex also demonstrate peripubertal changes that may influence cortical processing and plasticity.”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Fung et al., 2010
Cites
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
Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex
The Petilla Interneuron Nomenclature Group (PING) (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2402 · Cited by 1,491 · 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
Origin of GABAergic neurons in the human neocortex
Letinić, K., Zoncu, R., & RAKIC, P. T. (2002) · Nature · doi:10.1038/nature00779 · Cited by 718 · 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
Lieberman, J. A., Perkins, D. O., Belger, A., Chakos, M., Jarskog, F., Boteva, K., & Gilmore, J. H. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01303-8 · Cited by 593 · see citing works
Fate mapping Nkx2.1‐lineage cells in the mouse telencephalon
Xu, Q., Tam, M., & Anderson, S. A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21529 · Cited by 560 · see citing works
Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J. B., Battiste, J., Johnson, J. E., Machold, R. P., & Fishell, G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4515-09.2010 · Cited by 559 · 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
Self-citationHashimoto, T., Arion, D., Unger, T., Maldonado-Avilés, J. G., Morris, H. M., Volk, D. W., Mirnics, K., & Lewis, D. A. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002011 · Cited by 490 · see citing works
Hashimoto, T., Bazmi, H. H., Mirnics, K., Wu, Q., Sampson, A. R., & Lewis, D. A. (2008) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.07081223 · Cited by 457 · see citing works
Fogarty, M., Grist, M., Gelman, D., Marín, O., Pachnis, V., & Kessaris, N. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1629-07.2007 · Cited by 412 · see citing works
A 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
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
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 · see citing works
Neuroplasticity of Neocortical Circuits in Schizophrenia
Lewis, D. A., & González‐Burgos, G. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301563 · Cited by 362 · see citing works
Alterations in Chandelier Neuron Axon Terminals in the Prefrontal Cortex of Schizophrenic Subjects
Pierri, J. N., Chaudry, A. S., Woo, T.-U. W., & Lewis, D. A. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.11.1709 · Cited by 294 · see citing works
Mellios, N., Huang, H.-S., Baker, S. P., Galdzicka, M., Ginns, E., & Akbarian, S. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.019 · Cited by 266 · see citing works
Brain-Derived Neurotrophic Factor Promotes Differentiation of Striatal GABAergic Neurons
Mizuno, K., Carnahan, J. F., & Nawa, H. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1250 · Cited by 255 · see citing works
Intraventricular administration of BDNF increases neuropeptide expression in newborn rat brain
Nawa, H., Pelleymounter, M., & Carnahan, J. F. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03751.1994 · Cited by 235 · see citing works
Chapter 3 The Developmental Integration of Cortical Interneurons into a Functional Network
Batista‐Brito, R., & Fishell, G. (2009) · Current Topics in Developmental Biology · doi:10.1016/s0070-2153(09)01203-4 · Cited by 223 · see citing works
Volk, D. W., Austin, M. C., Pierri, J. N., Sampson, A. R., & Lewis, D. A. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.2.256 · Cited by 221 · see citing works
Morris, H. M., Hashimoto, T., & Lewis, D. A. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm186 · Cited by 213 · 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
Self-citationHof, P. R., & Morrison, J. H. (1991) · Experimental Neurology · doi:10.1016/0014-4886(91)90096-u · Cited by 196 · 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
Nawa, H., Bessho, Y., Carnahan, J. F., Nakanishi, S., & Mizuno, K. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb03216.x · Cited by 179 · see citing works
Duncan, C. E., Webster, M. J., Rothmond, D. A., Bahn, S., Elashoff, M., & Shannon Weickert, C. (2010) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2009.12.007 · Cited by 169 · see citing works
Self-citationGABAergic 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
Development of cortical GABAergic circuits and its implications for neurodevelopmental disorders
Cristo, G. D. (2007) · Clinical Genetics · doi:10.1111/j.1399-0004.2007.00822.x · Cited by 131 · see citing works
Origins of Cortical GABAergic Neurons in the Cynomolgus Monkey
Petanjek, Z., Berger, B., & Esclapez, M. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn078 · Cited by 130 · 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
Fertuzinhos, S., Krsnik, Ž., Kawasawa, Y. I., Rašin, M.-R., Kwan, K. Y., Chen, J.-G., Judaš, M., Hayashi, M., & Šestan, N. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp009 · Cited by 106 · see citing works
Selection of Reference Gene Expression in a Schizophrenia Brain Cohort
Weickert, C. S., Sheedy, D. L., Rothmond, D. A., Dedova, I. V., Fung, S. J., Garrick, T. M., Wong, J., Harding, A. J., Sivagnanansundaram, S., Hunt, C. E., et al. (2010) · Australian & New Zealand Journal of Psychiatry · doi:10.3109/00048670903393662 · Cited by 106 · see citing works
Self-citationGlorioso, C. A., Sabatini, M., Unger, T. L., Hashimoto, T., Monteggia, L. M., Lewis, D. A., & Mirnics, K. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001835 · Cited by 100 · see citing works
Transcriptome analysis of male–female differences in prefrontal cortical development
Weickert, C. S., Elashoff, M. R., Richards, A., Sinclair, D., Bahn, S., Pääbo, S., Khaitovich, P., & Webster, M. J. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.5 · Cited by 86 · see citing works
Self-citationHayes, T. L., & Lewis, D. A. (1992) · Cerebral Cortex · doi:10.1093/cercor/2.1.56 · Cited by 80 · see citing works
Neurons expressing calcium-binding proteins in the prefrontal cortex in schizophrenia
Tooney, P. A., & Chahl, L. A. (2004) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2003.10.004 · Cited by 63 · 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
de Belleroche, J., Bandopadhyay, R., King, A. J., et al. (1990) · Neuropeptides · doi:10.1016/0143-4179(90)90014-p · Cited by 46 · see citing works
Ontogeny of somatostatin in cerebral cortex of macaque monkey: an immunohistochemical study
Yamashita, A., Hayashi, M., Shimizu, K., & Oshima, K. (1989) · Developmental Brain Research · doi:10.1016/0165-3806(89)90012-6 · Cited by 46 · see citing works
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Larsen, B., & Luna, B. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.005 · Cited by 853 · see citing works
Neurodevelopmental model of schizophrenia: update 2012
Rapoport, J. L., Giedd, J. N., & Gogtay, N. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.23 · Cited by 790 · see citing works
Fillman, S. G., Cloonan, N., Catts, V. S., Miller, L. C., Wong, J., McCrossin, T., Cairns, M., & Weickert, C. S. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.110 · Cited by 609 · see citing works
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Caballero, A., Granberg, R., & Tseng, K. Y. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.013 · Cited by 357 · 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
Fillman, S. G., Sinclair, D., Fung, S. J., Webster, M. J., & Shannon Weickert, C. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.8 · Cited by 226 · see citing works
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Lewis, D. A. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.11.003 · Cited by 217 · see citing works
Canetta, S., Bolkan, S., Padilla-Coreano, N., Song, L. J., Sahn, R., Harrison, N. L., Gordon, J. A., Brown, A., & Kellendonk, C. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.222 · Cited by 201 · see citing works
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Catts, V. S., Fung, S. J., Long, L. E., Joshi, D., Vercammen, A., Allen, K. M., Fillman, S. G., Rothmond, D. A., Sinclair, D., Tiwari, Y., et al. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00060 · Cited by 206 · see citing works
Self-citationDeidda, G., Bozarth, I. F., & Cancedda, L. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00119 · Cited by 192 · see citing works
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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
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Abbas, A. I., Sundiang, M. J. M., Henoch, B., Morton, M. P., Bolkan, S. S., Park, A. J., Harris, A. Z., Kellendonk, C., & Gordon, J. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.029 · Cited by 183 · see citing works
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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 · see citing works
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Yanagi, M., Joho, R. H., Southcott, S. A., Shukla, A. A., Ghose, S., & Tamminga, C. A. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.49 · Cited by 102 · see citing works
Developmental changes in human dopamine neurotransmission: cortical receptors and terminators
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Self-citationPrenatal stress and inhibitory neuron systems: implications for neuropsychiatric disorders
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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
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Gill, K. M., & Grace, A. A. (2014) · The International Journal of Neuropsychopharmacology · doi:10.1017/s146114571400056x · Cited by 60 · see citing works
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Georgiev, D., Arion, D., Enwright, J. F., Kikuchi, M., Minabe, Y., Corradi, J. P., Lewis, D. A., & Hashimoto, T. (2014) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2013.13040468 · Cited by 61 · see citing works
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Self-citationCurley, A. A., Eggan, S. M., Lazarus, M. S., Huang, Z. J., Volk, D. W., & Lewis, D. A. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.10.018 · Cited by 51 · see citing works
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Wong, J., Duncan, C. E., Beveridge, N. J., Webster, M. J., Cairns, M. J., & Shannon Weickert, C. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr177 · Cited by 43 · see citing works
Self-citationMorishita, H., Kundakovic, M., Bicks, L., Mitchell, A., & Akbarian, S. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.03.005 · Cited by 42 · see citing works
Bristow, G. C., Thomson, D. M., Openshaw, R. L., Mitchell, E. J., Pratt, J. A., Dawson, N., & Morris, B. J. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107536 · Cited by 36 · see citing works
Tan, T., Wang, W., Williams, J., Ma, K., Cao, Q., & Yan, Z. (2019) · Schizophrenia Bulletin · doi:10.1093/schbul/sby163 · Cited by 29 · see citing works
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Reynolds, L. M., Faure, P., & Barik, J. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03110-0 · Cited by 26 · see citing works
Pujol, N., Penadés, R., Rametti, G., Catalán, R., Vidal-Piñeiro, D., Palacios, E., Bargallo, N., Bernardo, M., & Junqué, C. (2013) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2013.06.008 · Cited by 21 · see citing works
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- Authors
- Fung, S. J., Webster, M. J., Sivagnanasundaram, S., Duncan, C., Elashoff, M., & Weickert, C. S.
- Affiliations
- UNSW Sydney (AU)
- Venue
- American Journal of Psychiatry
- Published
- 2010-12
- Volume
- 167
- Issue
- 12
- Pages
- 1479-1488
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- OpenAlex
- W2125788186
- Cited by
- 366
- References
- 41
- Citations by year
- 2026: 10 · 2025: 20 · 2024: 21 · 2023: 18 · 2022: 14 · 2021: 28 · 2020: 19 · 2019: 21 · 2018: 29 · 2017: 21 · 2016: 30 · 2015: 25 · 2014: 31 · 2013: 33 · 2012: 28
- FWCI
- 17.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- 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, interneurons, dorsolateral prefrontal cortex, postnatal brain development, parvalbumin, somatostatin, cholecystokinin, calretinin, calbindin, neuropeptide Y, vasoactive intestinal peptide, GABAergic system, gene expression, neurodevelopmental hypothesis
- MeSH terms
- Adolescent, Adult, Brain, Child, Child, Preschool, Humans, Infant, Interneurons, Middle Aged, Neuropeptides, Parvalbumins, Schizophrenia, Prefrontal Cortex, Gene Expression Regulation, Developmental
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 ›
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