Postnatal Phencyclidine Administration Selectively Reduces Adult Cortical Parvalbumin-Containing Interneurons

Wang, Cheng Z; Yang, San F; Xia, Yan; Johnson, Kenneth M

doi:10.1038/sj.npp.1301647

Cited by 161Anesthesia and Neurotoxicity ResearchSchizophrenia research and treatmentNeuroscience and Neuropharmacology Research

Postnatal Phencyclidine Administration Selectively Reduces Adult Cortical Parvalbumin-Containing Interneurons

Wang, Cheng Z, Yang, San F, Xia, Yan, Johnson, Kenneth M·2008·Neuropsychopharmacology

DOI 10.1038/sj.npp.1301647

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Abstract

Transient postnatal NMDA receptor blockade by phencyclidine (PCP), ketamine, or MK-801 induces developmental neuroapoptosis and adult behavioral deficits, which resemble abnormal human behaviors typically present in schizophrenia. This study tested the hypothesis that PCP-induced developmental apoptosis causes a specific deficit of GABAergic interneurons containing parvalbumin (PV), calretinin (CR), or calbindin (CB). Young adult (PND56) rats that were given a single dose of PCP (10 mg/kg) on PND7 exhibited no densitometric change of either CR or CB neurons in any brain region studied, but demonstrated a selective deficit of PV-containing neurons in the superficial layers (II-IV) of the primary somatosensory (S1), motor (M), and retrosplenial cortices, but not in the striatum (CPu) or hippocampus. Further, CR and CB neurons, which were expressed at the time of PCP administration, showed no colocalization with cellular markers of apoptosis (terminal dUTP nick-end labeling (TUNEL) of broken DNA or cleaved caspase-3), indicating that CR- and CB-containing neurons were protected from the toxic effect of PCP and survived into adulthood. This suggests that the deletion of PV neurons occurred during development, but cleaved caspase-3 showed no colocalization with BrdU, a specific marker of S-phase proliferation. These data suggest that the loss of PV-containing neurons was not due to an effect of PCP on proliferating neurons, but rather an effect on post-mitotic neurons. The developmental dependence and neuronal specificity of this effect of PCP provides further evidence that this model may be valuable in exploring the pathophysiology of schizophrenia.

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Parvalbumin interneurons are especially vulnerable to NMDAR hypofunction during development.
“However, PVI are especially vulnerable to NMDAR hypofunction during development (Abekawa et al., 2007; Powell et al., 2012; Wang et al., 2008; Wang et al., 2013).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Wang et al., 2008
Early postnatal PCP reduces the number of adult PV+ neurons in the PFC.
“early postnatal PCP reduces the number of adult PVþ neurons in the PFC.58”
From Adolescent Onset of Cortical Disinhibition in Schizophrenia: Insights From Animal Models (2011) · cites this paper as [58]

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Ketamine-Induced Loss of Phenotype of Fast-Spiking Interneurons Is Mediated by NADPH-Oxidase
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Oxidative stress-driven parvalbumin interneuron impairment as a common mechanism in models of schizophrenia
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Highly energized inhibitory interneurons are a central element for information processing in cortical networks.
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Interleukin-6 Mediates the Increase in NADPH-Oxidase in the Ketamine Model of Schizophrenia
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Multiple origins of the cortical gamma rhythm
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Involvement of NOX2 in the Development of Behavioral and Pathologic Alterations in Isolated Rats
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Redox Dysregulation Affects the Ventral But Not Dorsal Hippocampus: Impairment of Parvalbumin Neurons, Gamma Oscillations, and Related Behaviors
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Ketamine and phencyclidine: the good, the bad and the unexpected
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Glutamatergic Synaptic Dysregulation in Schizophrenia: Therapeutic Implications
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Neuroinflammation and Oxidative Stress in Psychosis and Psychosis Risk
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NMDA receptor antagonist rodent models for cognition in schizophrenia and identification of novel drug treatments, an update
Cadinu, D., Grayson, B., Podda, G., Harte, M., Doostdar, N., & Neill, J. C. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.11.045 · Cited by 166 · see citing works
Downregulation of Parvalbumin at Cortical GABA Synapses Reduces Network Gamma Oscillatory Activity
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Behavioral and neurochemical consequences of cortical oxidative stress on parvalbumin-interneuron maturation in rodent models of schizophrenia
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
Does schizophrenia arise from oxidative dysregulation of parvalbumin-interneurons in the developing cortex?
Behrens, M. M., & B, T. J. S. A. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.06.002 · Cited by 160 · see citing works
NMDAR Hypofunction Animal Models of Schizophrenia
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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
Mechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
Alterations of prefrontal cortex GABAergic transmission in the complex psychotic-like phenotype induced by adolescent delta-9-tetrahydrocannabinol exposure in rats
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The Role of Parvalbumin Interneurons in Neurotransmitter Balance and Neurological Disease
Nahar, L., Delacroix, B. M., & Nam, H. W. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.679960 · Cited by 113 · see citing works
Spatial and temporal boundaries of NMDA receptor hypofunction leading to schizophrenia
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Cortical Oscillations in Health and Disease
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Glutamate and microglia activation as a driver of dendritic apoptosis: a core pathophysiological mechanism to understand schizophrenia
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Periadolescent Exposure to the NMDA Receptor Antagonist MK-801 Impairs the Functional Maturation of Local GABAergic Circuits in the Adult Prefrontal Cortex
Thomases, D. R., Cass, D. K., & Tseng, K. Y. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4147-12.2013 · Cited by 89 · see citing works
Convergence of genetic and environmental factors on parvalbumin-positive interneurons in schizophrenia
Jiang, Z., Cowell, R. M., & Nakazawa, K. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00116 · Cited by 89 · see citing works
Evidence for a neuroinflammatory mechanism in delayed effects of early life adversity in rats: Relationship to cortical NMDA receptor expression
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A loss of hippocampal perineuronal nets produces deficits in dopamine system function: relevance to the positive symptoms of schizophrenia
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
Dizocilpine (MK-801) induces distinct changes of N-methyl-d-aspartic acid receptor subunits in parvalbumin-containing interneurons in young adult rat prefrontal cortex
Dong, X., Zhang, W., Wang, H.-X., Stradtman, G. G., & Gao, W. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s146114570900042x · Cited by 82 · see citing works
Prefrontal Cortical Gamma-Aminobutyric Acid Transmission and Cognitive Function: Drawing Links to Schizophrenia from Preclinical Research
Tse, M., Piantadosi, P. T., & Floresco, S. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.09.007 · Cited by 73 · see citing works
mGluR1, but not mGluR5, activates feed-forward inhibition in the medial prefrontal cortex to impair decision making
Sun, H., & Neugebauer, V. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00762.2010 · Cited by 71 · see citing works
Inhibitory Interneurons, Oxidative Stress, and Schizophrenia
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Selective reorganization of GABAergic transmission in neonatal ventral hippocampal-lesioned rats
François, J., Ferrandon, A., Koning, E., Angst, M.-J., Sandner, G., & Nehlig, A. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709009985 · Cited by 68 · see citing works
Mice with genetically altered glutamate receptors as models of schizophrenia: A comprehensive review
Inta, D., Monyer, H., Sprengel, R., Meyer‐Lindenberg, A., & Gass, P. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.07.010 · Cited by 67 · see citing works
Neurodevelopmental Animal Models of Schizophrenia: Role in Novel Drug Discovery and Development
Wilson, C., & Terry, A. V. (2010) · Clinical Schizophrenia & Related Psychoses · doi:10.3371/csrp.4.2.4 · Cited by 66 · see citing works
Sex differences in animal models of schizophrenia shed light on the underlying pathophysiology
Hill, R. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.10.014 · Cited by 61 · see citing works
A “double hit” murine model for schizophrenia shows alterations in the structure and neurochemistry of the medial prefrontal cortex and the hippocampus
Gilabert‐Juan, J., Bellés, M., Sáez-Ibáñez, A. R., Carceller, H., Zamarbide-Forés, S., Moltó, M. D., & Nácher, J. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.07.008 · Cited by 53 · see citing works
Neonatal phencyclidine administration and post-weaning social isolation as a dual-hit model of ‘schizophrenia-like’ behaviour in the rat
Gaskin, P. L. R., Alexander, S. P. H., & Fone, K. C. F. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3424-y · Cited by 51 · see citing works
Excitatory and inhibitory neurotransmission is chronically altered following perinatal NMDA receptor blockade
du Bois, T. M., Deng, C., Han, M., Newell, K. A., & Huang, X. (2009) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.12.002 · Cited by 50 · see citing works
Interneuron Transcriptional Dysregulation Causes Frequency-Dependent Alterations in the Balance of Inhibition and Excitation in Hippocampus
Bartley, A. F., Lucas, E. K., Brady, L. J., Li, Q., Hablitz, J. J., Cowell, R. M., & Dobrunz, L. E. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1834-15.2015 · Cited by 50 · see citing works
Reciprocal signalling between NR2 subunits of the NMDA receptor and neuregulin1 and their role in schizophrenia
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Postnatal Phencyclidine (PCP) as a Neurodevelopmental Animal Model of Schizophrenia Pathophysiology and Symptomatology: A Review
Grayson, B., Barnes, S. A., Markou, A., Piercy, C., Podda, G., & Neill, J. C. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_403 · Cited by 48 · see citing works
How Nox2-Containing NADPH Oxidase Affects Cortical Circuits in the NMDA Receptor Antagonist Model of Schizophrenia
Wang, X., Pinto-Duarte, A., Sejnowski, T. J., & Behrens, M. M. (2013) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.4907 · Cited by 46 · see citing works
NMDA receptor-dependent function and plasticity in inhibitory circuits
Moreau, A. W., & Kullmann, D. M. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.004 · Cited by 44 · see citing works
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Down-Regulation of Hippocampal Genes Regulating Dopaminergic, GABAergic, and Glutamatergic Function Following Combined Neonatal Phencyclidine and Post-Weaning Social Isolation of Rats as a Neurodevelopmental Model for Schizophrenia
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Perinatal phencyclidine treatment alters neuregulin 1/erbB4 expression and activation in later life
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Repeated Neonatal Sevoflurane Exposure-Induced Developmental Delays of Parvalbumin Interneurons and Cognitive Impairments Are Reversed by Environmental Enrichment
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The impact of adolescent social isolation on dopamine D2 and cannabinoid CB1 receptors in the adult rat prefrontal cortex
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Long-term effects of neonatal exposure to MK-801 on recognition memory and excitatory–inhibitory balance in rat hippocampus
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Subchronic phencyclidine treatment in adult mice increases GABAergic transmission and LTP threshold in the hippocampus
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Post-weaning social isolation and subchronic NMDA glutamate receptor blockade: Effects on locomotor activity and GABA signaling in the rat suggest independent mechanisms
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Downregulation of Npas4 in parvalbumin interneurons and cognitive deficits after neonatal NMDA receptor blockade: relevance for schizophrenia
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Postnatal exposure to MK801 induces selective changes in GAD67 or parvalbumin
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Local injection of MK801 modifies oscillatory activity in the nucleus accumbens in awake rats
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Prolonged exposure to NMDAR antagonist induces cell-type specific changes of glutamatergic receptors in rat prefrontal cortex
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Authors: Wang, C. Z., Yang, S. F., Xia, Y., & Johnson, K. M.
Affiliations: The University of Texas Medical Branch at Galveston (US)
Corresponding author: Wang, Cheng Z
Johnson, Kenneth M
ORCID: Xia, Yan
Venue: Neuropsychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2007-12-05
Volume: 33
Issue: 10
Pages: 2442-2455
ISSN: 0893-133X (ISSN-L)
1740-634X
DOI: 10.1038/sj.npp.1301647
OpenAlex: W2026782090
Cited by: 161
References: 110
Citations by year: 2026: 1 · 2025: 5 · 2024: 1 · 2023: 2 · 2022: 1 · 2021: 3 · 2020: 4 · 2019: 9 · 2018: 6 · 2017: 9 · 2016: 6 · 2015: 13 · 2014: 13 · 2013: 11 · 2012: 7
FWCI: 5.48
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Neuropsychopharmacology (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Department of Health and Human Services
University of Texas Medical Branch
National Institutes of Health (5r01mh063871-04)
National Institute of Mental Health (MH63871)
National Institute on Drug Abuse (DA 02073, R01DA002073)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Anesthesia and Neurotoxicity Research
Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: phencyclidine, NMDA receptor blockade, parvalbumin interneurons, calretinin, calbindin, GABAergic interneurons, schizophrenia model, postnatal drug exposure, caspase-3, TUNEL, somatosensory cortex, motor cortex, retrosplenial cortex
MeSH terms: Animals, Animals, Newborn, Bromodeoxyuridine, Cell Count, Cell Survival, Cerebral Cortex, Disease Models, Animal, Female, Interneurons, Male, Parvalbumins, Phencyclidine, Schizophrenia, Time, Rats, Sprague-Dawley, Apoptosis, Excitatory Amino Acid Antagonists, Cell Proliferation, Rats, Caspase 3, Calbindins, S100 Calcium Binding Protein G, Calbindin 2

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Postnatal Phencyclidine Administration Selectively Reduces Adult Cortical Parvalbumin-Containing Interneurons

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