Oxidative stress-driven parvalbumin interneuron impairment as a common mechanism in models of schizophrenia
Open accessAbstract
Parvalbumin inhibitory interneurons (PVIs) are crucial for maintaining proper excitatory/inhibitory balance and high-frequency neuronal synchronization. Their activity supports critical developmental trajectories, sensory and cognitive processing, and social behavior. Despite heterogeneity in the etiology across schizophrenia and autism spectrum disorder, PVI circuits are altered in these psychiatric disorders. Identifying mechanism(s) underlying PVI deficits is essential to establish treatments targeting in particular cognition. On the basis of published and new data, we propose oxidative stress as a common pathological mechanism leading to PVI impairment in schizophrenia and some forms of autism. A series of animal models carrying genetic and/or environmental risks relevant to diverse etiological aspects of these disorders show PVI deficits to be all accompanied by oxidative stress in the anterior cingulate cortex. Specifically, oxidative stress is negatively correlated with the integrity of PVIs and the extracellular perineuronal net enwrapping these interneurons. Oxidative stress may result from dysregulation of systems typically affected in schizophrenia, including glutamatergic, dopaminergic, immune and antioxidant signaling. As convergent end point, redox dysregulation has successfully been targeted to protect PVIs with antioxidants/redox regulators across several animal models. This opens up new perspectives for the use of antioxidant treatments to be applied to at-risk individuals, in close temporal proximity to environmental impacts known to induce oxidative stress.
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Written from the paper’s full text.
TL;DR
This review and new comparative analysis argues that oxidative stress is a common pathological mechanism driving parvalbumin interneuron (PVI) and perineuronal net (PNN) deficits in schizophrenia and some autism models. Across diverse genetic and environmental rodent models, PVI/PNN loss in anterior cingulate cortex was accompanied by oxidative stress, and antioxidant/redox-regulator treatment protected PVIs in several models.
Key findings
- In the anterior cingulate cortex, increased oxidative stress (8-oxo-dG) was consistently accompanied by reduced PV-immunoreactive cells and WFA-labeled PNNs across many models: 22q11 deletion (+125% 8-oxo-dG, −22% PV-IR cells, −38% PNN), 15q13.3 deletion (+262%, −35%, −45%), FMR1 KO (+307%, −48%, −50%), SRR KO (+410%, −26%, −35%), two-hit poly(I:C)/stress (+190%, −38%, −63%), NVHL rats (+450%, −43%, −55%), and MAM rats (+164%, −44%, −49%).
- Some models lacked significant oxidative stress and PVI/PNN deficits at baseline: 1q21 deletion and GRIN2A KO mice; GCLM KO mice showed small oxidative stress (+53% 8-oxo-dG) but no PVI/PNN deficit. However, GRIN2A KO and GCLM KO mice became susceptible to early postnatal oxidative challenge (GBR), showing long-lasting oxidative stress and PVI/PNN deficits (GRIN2A: +159%, −17%, −36%; GCLM: +127%, −44%, −52%).
- Across all investigated animal models, increased oxidative stress correlated negatively with relative decreases in PV-IR cells and PV-IR cells with PNN, and decreases in PV-IR cells correlated strongly with PNN decreases.
- Antioxidants/redox regulators protected PVIs in several models (GBR-treated GCLM mice, ketamine-treated mice, isolated rats, isolated mice with NR1 deletion in forebrain interneurons, socially defeated rats, and NVHL rats), and oxidative stress preceded PVI deficit in hippocampus, supporting a causal role.
Methods
- The paper reviews published data and presents new comparative immunohistological analyses of oxidative stress and PVI integrity in the anterior cingulate cortex across genetic and/or environmental rodent models relevant to schizophrenia and autism.
- Oxidative stress was detected with an antibody against 8-oxo-2′-deoxyguanosine (8-oxo-dG); PVI integrity was assessed with anti-parvalbumin and Wisteria floribunda agglutinin (WFA) to label the perineuronal net.
- Analyses were performed in late adolescent/young adult animals (2–3 months old); models included human copy number variation mice (22q11, 15q13, 1q21), gene knockouts (FMR1, SRR, GRIN2A), glutathione-deficiency models (GCLM KO, PV:GCLC KO, transient GSH depletion), gene–environment interaction models, a two-hit immune/stress model, and NVHL and MAM rat models.
Limitations
- The paper states that the hypothesis should be further tested in other models, that the mechanisms causing oxidative stress are unlikely to be similar across all models, and that the analysis focused on prefrontal cortex although other brain regions may be affected.
- The paper states that preventive antioxidant intervention will require reliable biomarkers for brain oxidative stress/redox dysregulation and PVI function in high-risk individuals.
- Evident from the text: much of the evidence is correlational across models, with causal support coming mainly from antioxidant rescue and temporal precedence in some models rather than all; no human clinical trial data are presented.
Model-written summary. Check it against the paper before relying on it.
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Cites
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Claims the paper makes
0 of 28 cited sources checked · 0 supported · 0 flagged
- Findingcitation
Redox dysregulation has successfully been targeted to protect PVIs with antioxidants/redox regulators across several animal models.
“As convergent end point, redox dysregulation has successfully been targeted to protect PVIs with antioxidants/redox regulators across several animal models.”
Quote in the paperSubstantial claim0 of 6 sources checked- cites [39] Cabungcal JH, Steullet P, Kraftsik R, Cuenod M, Do KQ . Early-life insults impair parvalbumin interneurons via oxidative stress: reversal by N-acetylcysteine. Biol Psychiatry 2013; 73: 574–582. source
Not checked in the free run.
- cites [37] Behrens MM, Ali SS, Dao DN, Lucero J, Shekhtman G, Quick KL et al. Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 2007; 318: 1645–1647. source
Not checked in the free run.
- cites [23] Schiavone S, Sorce S, Dubois-Dauphin M, Jaquet V, Colaianna M, Zotti M et al. Involvement of NOX2 in the development of behavioral and pathologic alterations in isolated rats. Biol Psychiatry 2009; 66: 384–392. source
Not checked in the free run.
- cites [83] Jiang Z, Rompala GR, Zhang S, Cowell RM, Nakazawa K . Social isolation exacerbates schizophrenia-like phenotypes via oxidative stress in cortical interneurons. Biol Psychiatry 2013; 73: 1024–1034. source
Not checked in the free run.
- cites [84] Bouvier E, Brouillard F, Molet J, Claverie D, Cabungcal JH, Cresto N et al. Nrf2-dependent persistent oxidative stress results in stress-induced vulnerability to depression. Mol Psychiatry 2016 advance online publication, 20 September 2016; doi:10.1038/mp.2016.144. source
Not checked in the free run.
- cites [41] Cabungcal JH, Counotte DS, Lewis EM, Tejeda HA, Piantadosi P, Pollock C et al. Juvenile antioxidant treatment prevents adult deficits in a developmental model of schizophrenia. Neuron 2014; 83: 1073–1084. source
Not checked in the free run.
- Findingown data
A series of animal models carrying genetic and/or environmental risks relevant to schizophrenia and ASD show PVI deficits all accompanied by oxidative stress in the anterior cingulate cortex.
“A series of animal models carrying genetic and/or environmental risks relevant to diverse etiological aspects of these disorders show PVI deficits to be all accompanied by oxidative stress in the anterior cingulate cortex.”
Quote in the paperSubstantial claim - Findingnone given
Oxidative stress is negatively correlated with the integrity of PVIs and the extracellular perineuronal net enwrapping these interneurons.
“Specifically, oxidative stress is negatively correlated with the integrity of PVIs and the extracellular perineuronal net enwrapping these interneurons.”
Quote in the paperSubstantial claim - Findingown data
Overall, PVI deficit in the ACC was in all cases accompanied by oxidative stress.
“Overall, our analysis remarkably demonstrates that PVI deficit in the ACC was in all cases accompanied by oxidative stress.”
Quote in the paperSubstantial claim - Findingown data
Considering all investigated animal models, increased oxidative stress correlated negatively with the relative decreased number of PV-IR cells or PV-IR cells with PNN.
“Considering all investigated animal models, increased oxidative stress correlated negatively with the relative decreased number of PV-IR cells or PV-IR cells with PNN (Figure 1b), suggesting a direct link between oxidative stress and PVI anomalies.”
Quote in the paperSubstantial claim
- Premisecitation
PVIs are vulnerable to redox dysregulation/oxidative stress.
“Indeed, PVIs are vulnerable to redox dysregulation/oxidative stress.37, 38, 39, 40”
Quote in the paperSubstantial claim0 of 4 sources checked- cites [37] Behrens MM, Ali SS, Dao DN, Lucero J, Shekhtman G, Quick KL et al. Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 2007; 318: 1645–1647. source
Not checked in the free run.
- cites [38] Cabungcal JH, Nicolas D, Kraftsik R, Cuenod M, Do KQ, Hornung JP . Glutathione deficit during development induces anomalies in the rat anterior cingulate GABAergic neurons: relevance to schizophrenia. Neurobiol Dis 2006; 22: 624–637. source
Not checked in the free run.
- cites [39] Cabungcal JH, Steullet P, Kraftsik R, Cuenod M, Do KQ . Early-life insults impair parvalbumin interneurons via oxidative stress: reversal by N-acetylcysteine. Biol Psychiatry 2013; 73: 574–582. source
Not checked in the free run.
- cites [40] Morishita H, Cabungcal JH, Chen Y, Do KQ, Hensch TK . Prolonged period of cortical plasticity upon redox dysregulation in fast-spiking interneurons. Biol Psychiatry 2015; 78: 396–402. source
Not checked in the free run.
- Premisecitation
Both increase and decrease in the number of PV-IR cells are reported in these models.
“Both increase and decrease in number of PV-IR cells are reported.”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [27] Filice F, Vorckel KJ, Sungur AO, Wohr M, Schwaller B . Reduction in parvalbumin expression not loss of the parvalbumin-expressing GABA interneuron subpopulation in genetic parvalbumin and shank mouse models of autism. Mol Brain 2016; 9: 10. source
Not checked in the free run.
- cites [28] Penagarikano O, Abrahams BS, Herman EI, Winden KD, Gdalyahu A, Dong H et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell 2011; 147: 235–246. source
Not checked in the free run.
- cites [113] Cellot G, Cherubini E . Reduced inhibitory gate in the barrel cortex of Neuroligin3R451C knock-in mice, an animal model of autism spectrum disorders. Physiol Rep 2014; 2: e12077. source
Not checked in the free run.
- Interpretationnone given
Aberrant migration of interneuron precursors and perturbed positioning of PVIs within cortical circuits due to genetic and/or prenatal environmental factors may be mediated by mechanisms independent of oxidative stress.
“In contrast, aberrant migration of interneuron precursors and perturbed positioning of PVIs within the cortical circuits due to genetic and/or prenatal environmental factors may be mediated by mechanisms independent of oxidative stress.”
Quote in the paperNot a substantial claim - Premisecitation
Manipulations of other genes associated with intellectual disability and ASD (e.g., MECP2, NLGN3, Shank3, CNTNAP2) reveal diverse abnormalities within cortical GABAergic circuits.
“Manipulations of other genes associated with intellectual disability and ASD (for example, MECP2, NLGN3, Shank3; CNTNAP2) reveal diverse abnormalities within cortical GABAergic circuits.27, 28, 113, 114, 115”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [27] Filice F, Vorckel KJ, Sungur AO, Wohr M, Schwaller B . Reduction in parvalbumin expression not loss of the parvalbumin-expressing GABA interneuron subpopulation in genetic parvalbumin and shank mouse models of autism. Mol Brain 2016; 9: 10. source
Not checked in the free run.
- cites [28] Penagarikano O, Abrahams BS, Herman EI, Winden KD, Gdalyahu A, Dong H et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell 2011; 147: 235–246. source
Not checked in the free run.
- cites [113] Cellot G, Cherubini E . Reduced inhibitory gate in the barrel cortex of Neuroligin3R451C knock-in mice, an animal model of autism spectrum disorders. Physiol Rep 2014; 2: e12077. source
Not checked in the free run.
- Premisenone given
Peri-adolescent administration of antioxidants can restore or protect PVI integrity in some animal models.
“The fact that peri-adolescent administration of antioxidants can restore or protect PVI integrity in some animal models provides a strong support that early antioxidant-based treatments might be beneficial to PVI-associated networks.”
Quote in the paperSubstantial claim - Interpretationreasoning
In contrast to schizophrenia models, there is no convergent mechanism responsible for PVI anomalies in ASD-relevant models.
“In contrast to the schizophrenia models, this suggests no convergent mechanism responsible for PVI anomalies in ASD relevant models.”
Quote in the paperSubstantial claim - Interpretationcitation
The oxidative stress-induced PVI deficit may also hold for other brain regions like the hippocampus, as shown in some models of schizophrenia (e.g., GCLM KO, ketamine, MAM, poly(I:C), and social defeat).
“Although our analysis focused on oxidative stress-induced PVI deficit in the prefrontal cortex, this deficit may also hold for other brain regions like the hippocampus, as shown in some models of schizophrenia (for example, GCLM KO, ketamine, MAM, poly(I:C) and social defeat.22, 37, 47, 48, 84”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [22] Meyer U, Nyffeler M, Yee BK, Knuesel I, Feldon J . Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav Immun 2008; 22: 469–486. source
Not checked in the free run.
- cites [37] Behrens MM, Ali SS, Dao DN, Lucero J, Shekhtman G, Quick KL et al. Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 2007; 318: 1645–1647. source
Not checked in the free run.
- cites [47] Steullet P, Cabungcal JH, Kulak A, Kraftsik R, Chen Y, Dalton TP et al. Redox dysregulation affects the ventral but not dorsal hippocampus: impairment of parvalbumin neurons, gamma oscillations, and related behaviors. J Neurosci 2010; 30: 2547–2558. source
Not checked in the free run.
- Interpretationreasoning
GSH deficiency confers a vulnerability to oxidative stress-induced PVI impairment.
“Together, this demonstrates that a GSH deficiency confers a vulnerability to oxidative stress-induced PVI impairment.”
Quote in the paperSubstantial claim - Interpretationreasoning
Oxidative stress is a common pathological mechanism leading to PVI impairment in schizophrenia and some forms of autism.
“we propose oxidative stress as a common pathological mechanism leading to PVI impairment in schizophrenia and some forms of autism.”
Quote in the paperSubstantial claim - Premisecitation
PVI circuits are altered in schizophrenia and autism spectrum disorder despite heterogeneity in etiology.
“Despite heterogeneity in the etiology across schizophrenia and autism spectrum disorder, PVI circuits are altered in these psychiatric disorders.”
- Also stated in: § Abstract · boosted
“alterations in parvalbumin-expressing interneurons (PVIs) are highly replicated findings in postmortem brains of schizophrenia patients,6, 7 and are reported in bipolar (BP)8 and autism spectrum disorders (ASD).9”
Quote in the paperSubstantial claim0 of 4 sources checked- cites [6] Beasley CL, Reynolds GP . Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr Res 1997; 24: 349–355. source
Not checked in the free run.
- cites [7] Lewis DA, Curley AA, Glausier JR, Volk DW . Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci 2012; 35: 57–67. source
Not checked in the free run.
- cites [8] Sakai T, Oshima A, Nozaki Y, Ida I, Haga C, Akiyama H et al. Changes in density of calcium-binding-protein-immunoreactive GABAergic neurons in prefrontal cortex in schizophrenia and bipolar disorder. Neuropathology 2008; 28: 143–150. source
Not checked in the free run.
- cites [9] Hashemi E, Ariza J, Rogers H, Noctor SC, Martinez-Cerdeno V . The number of parvalbumin-expressing interneurons is decreased in the medial prefrontal cortex in autism. Cereb Cortex 2016. pii:bhw021. source
Not checked in the free run.
- Also stated in: § Abstract · boosted
- Interpretationnone given
Redox dysregulation/oxidative stress is a common pathological mechanism affecting prefrontal PVIs during postnatal maturation in a strikingly diversified number of models relevant to schizophrenia and some forms of ASD.
“Redox dysregulation/oxidative stress is a common pathological mechanism affecting prefrontal PVIs during postnatal maturation in a strikingly diversified number of models relevant to schizophrenia and some forms of ASD.”
Quote in the paperSubstantial claim - Interpretationreasoning
Oxidative stress could be the main agent responsible for PVI-associated network anomalies, particularly in schizophrenia.
“This confluence suggests that oxidative stress could be the main agent responsible for PVI-associated network anomalies particularly in schizophrenia.”
Quote in the paperSubstantial claim- Rests on an assumption: Animal models relevant to schizophrenia and some forms of ASD are valid models of the corresponding human disorders.
- Interpretationreasoning
Early antioxidant-based treatments might be beneficial to PVI-associated networks.
“The fact that peri-adolescent administration of antioxidants can restore or protect PVI integrity in some animal models provides a strong support that early antioxidant-based treatments might be beneficial to PVI-associated networks.”
Quote in the paperSubstantial claim
- May combine two claims. 4
- Classified as probably not a substantial claim. 3
May combine two claims.
PremisecitationShank1 and Shank3B knockout mice show a reduced number of PV-IR cells but no deficit in WFA-labeled perineuronal nets in the somatosensory cortex.
“Moreover, Shank1 and Shank3B KO mice show a reduced number of PV-IR cells but no deficit in WFA-labeled PNN in the somatosensory cortex.27”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [27] Filice F, Vorckel KJ, Sungur AO, Wohr M, Schwaller B . Reduction in parvalbumin expression not loss of the parvalbumin-expressing GABA interneuron subpopulation in genetic parvalbumin and shank mouse models of autism. Mol Brain 2016; 9: 10. source
Not checked in the free run.
Probably not a substantial claim: may not pass S2 (checkable). May combine two claims.
InterpretationreasoningSuch treatment could improve cognitive processing and ameliorate general functioning of patients.
“Knowing the role of PVIs in cognition and social behavior, this could improve cognitive processing and ameliorate general functioning of patients.”
Quote in the paperNot a substantial claim- Rests on an assumption: Animal models relevant to schizophrenia and some forms of ASD are valid models of the corresponding human disorders.
- Rests on an assumption: PVIs play a role in cognition and social behavior.
- Rests on an assumption: Findings in animal models about antioxidant effects on PVI integrity translate to human patients.
Probably not a substantial claim: may not pass S1 (asserted). May combine two claims.
InterpretationcitationRedox dysregulation/oxidative stress halts normal PVI maturation in the prefrontal cortex without causing their death, possibly via epigenetic mechanisms.
“Based on the fact that a peripubertal antioxidant treatment can abolish oxidative stress and rescue PVI/PNN deficit in the NVHL rat model,41 we propose a hypothesis in which redox dysregulation/oxidative stress halts normal PVI maturation in the prefrontal cortex without causing their death,82 possibly via epigenetic mechanisms.102, 103”
Quote in the paperNot a substantial claim0 of 4 sources checked- cites [41] Cabungcal JH, Counotte DS, Lewis EM, Tejeda HA, Piantadosi P, Pollock C et al. Juvenile antioxidant treatment prevents adult deficits in a developmental model of schizophrenia. Neuron 2014; 83: 1073–1084. source
Not checked in the free run.
- cites [82] Powell SB, Sejnowski TJ, Behrens MM . Behavioral and neurochemical consequences of cortical oxidative stress on parvalbumin-interneuron maturation in rodent models of schizophrenia. Neuropharmacology 2012; 62: 1322–1331. source
Not checked in the free run.
- cites [102] Fachim HA, Srisawat U, Dalton CF, Harte MK, Marsh S, Neill JC et al. Subchronic administration of phencyclidine produces hypermethylation in the parvalbumin gene promoter in rat brain. Epigenomics 2016; 8: 1179–1183. source
Not checked in the free run.
- cites [103] Morishita H, Kundakovic M, Bicks L, Mitchell A, Akbarian S . Interneuron epigenomes during the critical period of cortical plasticity: Implications for schizophrenia. Neurobiol Learn Mem 2015; 124: 104–110. source
Not checked in the free run.
Probably not a substantial claim: may not pass S1 (asserted), S4 (based). May combine two claims.
InterpretationreasoningAbnormal PVI-associated networks in schizophrenia and ASD has a neurodevelopmental origin and implicates redox dysregulation/oxidative stress.
“Our hypothesis that abnormal PVI-associated networks in schizophrenia and ASD has a neurodevelopmental origin and implicates redox dysregulation/oxidative stress should be however further tested in other models.”
Quote in the paperNot a substantial claim
The paper relies on this without support.
Animal models relevant to schizophrenia and some forms of ASD are valid models of the corresponding human disorders.
“Redox dysregulation/oxidative stress is a common pathological mechanism affecting prefrontal PVIs during postnatal maturation in a strikingly diversified number of models relevant to schizophrenia and some forms of ASD.”
The paper relies on this without support.
PVIs play a role in cognition and social behavior.
“Knowing the role of PVIs in cognition and social behavior”
The paper relies on this without support.
Findings in animal models about antioxidant effects on PVI integrity translate to human patients.
“The fact that peri-adolescent administration of antioxidants can restore or protect PVI integrity in some animal models provides a strong support that early antioxidant-based treatments might be beneficial to PVI-associated networks.”
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?
In animal models with no change in oxidative stress, PV-positive interneuron number was unchanged.
“Conversely, in animal models where no change in oxidative stress was observed, PV-positive interneuron number was not changed [92].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [92]
In rodent models of brain disorders, higher oxidative stress consistently correlates with fewer PV-positive cortical interneurons.
“In rodent models that recapitulate aspects of brain disorders, higher oxidative stress consistently correlates with decreased PV-positive cortical interneurons [92,93].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [92]
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Self-citationInterleukin-6 Mediates the Increase in NADPH-Oxidase in the Ketamine Model of Schizophrenia
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Self-citationParvalbumin Deficiency and GABAergic Dysfunction in Mice Lacking PGC-1α
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Biomarkers of Oxidative Stress and Antioxidant Defense
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Parvalbumin interneuron vulnerability and brain disorders
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“In rodent models that recapitulate aspects of brain disorders, higher oxidative stress consistently correlates with decreased PV-positive cortical interneurons [92, 93].”
BackgroundRegulation of neuronal development and function by ROS
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“An impairment of the neuroprotective effects may be involved in the pathology of the neurodevelopmental disorders [208-210].”
BackgroundSteullet, 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
“Data from several animal models relevant to SZ indicate that oxidative stress is a convergent mechanism inducing PV interneurons and WFA/PNNs impairment in the prefrontal cortex (55).”
BackgroundSelf-citationMaitra, M., Mitsuhashi, H., Rahimian, R., Chawla, A., Yang, J., Fiori, L. M., Davoli, M. A., Perlman, K., Aouabed, Z., Mash, D. C., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38530-5 · Cited by 164 · see citing works
“Oxidative and cellular stress relate to PV neuron and PNN de fi cits in animal models 62 and cellular stress may be part of the molecular pathology in MDD 63 .”
Reconceptualization of translocator protein as a biomarker of neuroinflammation in psychiatry
Notter, T., Coughlin, J. M., Sawa, A., & Meyer, U. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.232 · Cited by 142 · see citing works
Self-citationOxidative Stress and the Pathophysiology and Symptom Profile of Schizophrenia Spectrum Disorders
Murray, A., Rogers, J. C., Katshu, M. Z. U. H., Liddle, P. F., & Upthegrove, R. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.703452 · Cited by 147 · see citing works
“Furthermore, these knockout mice demonstrate neuronal changes within the hippocampus similar to those seen in schizophrenia, specifically decreasing the numbers of parvalbumin interneurons (67).”
BackgroundParvalbumin interneuron in the ventral hippocampus functions as a discriminator in social memory
Deng, X., Gu, L., Sui, N., Guo, J., & Liang, J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1819133116 · Cited by 125 · see citing works
“However, this explanation may be insufficient because long-term social isolation is also a type of chronic stress (37) and induces multiple alterations in the neural system, such as increased oxidative stress (27, 28, 38) and the down-regulation of brain-derived neurotrophic factor (36, 39).”
BackgroundDwir, D., Giangreco, B., Xin, L., Tenenbaum, L., Cabungcal, J.-H., Steullet, P., Goupil, A., Cleusix, M., Jenni, R., Chtarto, A., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0393-5 · Cited by 137 · see citing works
“Environmental factors known to favor major psychiatric disorders also generate reactive oxygen species (ROS) which, if the redox regulation is impaired, will perturb the developing nervous system [2, 12, 13].”
BackgroundSelf-citationWingert, J. C., & Sorg, B. A. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.673210 · Cited by 129 · see citing works
Cuénod, M., Steullet, P., Cabungcal, J.-H., Dwir, D., Khadimallah, I., Klauser, P., Conus, P., & Kim, Q. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01374-w · Cited by 129 · see citing works
“2 locus containing most proteins expressed in mitochondria [19] show increased cytoplasmic 8-oxo-2’-deoxyguanosine (suggesting mitochondrial DNA oxidation), reduced number of PV-immunoreactive interneurons, and weakened PNN in anterior cingulate cortex [15].”
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“We envision that the volumetric superresolution imaging platform reported here, which allows molecular imaging with nanometerscale resolution across large tissue volumes, can be applied to track the pathogenesis of a variety of mental illnesses linked to disruptions in neuronal networks and the extracellular matrix (5…”
Self-citationUpper cortical layer–driven network impairment in schizophrenia
Batiuk, M. Y., Tyler, T., Dragičević, K., Mei, S., Rydbirk, R., Petukhov, V., Deviatiiarov, R. M., Sedmak, D., Frank, E., Feher, V., et al. (2022) · Science Advances · doi:10.1126/sciadv.abn8367 · Cited by 141 · see citing works
“Besides function and morphology, their distribution across cortical layers and overall density in the cortex were also found altered (9, 10).”
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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 118 · see citing works
“As oxidative stress can contribute to mitochondrial deficits, one hypothesis is that oxidative stress is the pathological mechanism causing impairments in Pv-FSI exhibited in schizophrenia and other psychiatric disorders (94).”
BackgroundCattane, N., Richetto, J., & Cattaneo, A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.001 · Cited by 118 · see citing works
Reactive oxygen species regulate activity-dependent neuronal plasticity in Drosophila
Oswald, M. C. W., Brooks, P. S., Zwart, M., Mukherjee, A., West, R. J. H., Giachello, C. N., Morarach, K., Baines, R., Sweeney, S. T., & Landgraf, M. (2018) · eLife · doi:10.7554/elife.39393 · Cited by 111 · see citing works
“Recent studies have linked increased ROS levels with neurodevelopmental conditions such as schizophrenia, bipolar and autism spectrum disorders (Do et al., 2015; Steullet et al., 2017).”
BackgroundThe Parvalbumin Hypothesis of Autism Spectrum Disorder
Filice, F., Janickova, L., Henzi, T., Bilella, A., & Schwaller, B. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.577525 · Cited by 112 · see citing works
“(Clemente-Perez et al., 2017; Steullet et al., 2017a).”
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“ELS increases circulating stress hormones and pro-inflammatory cytokines via sexdependent mechanisms associated with oxidative damage to PV+ interneurons in the PFC (Steullet et al., 2017).”
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Potential Roles of Redox Dysregulation in the Development of Schizophrenia
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Protein-C Reactive as Biomarker Predictor of Schizophrenia Phases of Illness? A Systematic Review
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“Parvalbumin interneurons (PVIs), particularly through the hypofunction of N-methyl-D-aspartate receptors (NMDARs), are involved in the schizophrenic development [107].”
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Cytosolic Ca 2+ Buffers Are Inherently Ca 2+ Signal ModulatorsPreprint
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“…recently proposed as the pathological mechanism leading to parvalbumin expressing interneurons impairment in schizophrenia and some forms of autism [69]; and different neuronal activity has been observed between excitatory and subgroups of inhibitory neurons in the APP/PS1 mouse model of AD [70].”
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Fifty Years of Research on Schizophrenia: The Ascendance of the Glutamatergic Synapse
Coyle, J. T., Ruzicka, W. B., & Balu, D. T. (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.20101481 · Cited by 84 · see citing works
“They have significant memory impairments that are associated with frontal cortical (90), amygdala (91), and hippocampal dysfunction (89); significant cortical atrophy of 5% accompanied by a 20% increase in ventricular volume on quantitative MRI (92); a down-regulation of PV expression in cortical GABAergic neurons; lo…”
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Increased cortical reactivity to repeated tones at 8 months in infants with later ASD
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Obesity, altered oxidative stress, and clinical correlates in chronic schizophrenia patients
An, H., Du, X., Huang, X., Qi, L., Jia, Q., Yin, G., Xiao, C., Huang, X., Ning, Y., Cassidy, R. M., et al. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0303-7 · Cited by 80 · see citing works
Role of Hydrazine-Related Chemicals in Cancer and Neurodegenerative Disease
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Coenzyme Q10 a mitochondrial restorer for various brain disorders
Pradhan, N., Singh, C., & Singh, A. (2021) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-021-02161-8 · Cited by 77 · see citing works
“The nerve cell is especially vulnerable to oxidative threat due to very high degree of aerobic metabolism and presence of highly oxidizable molecules (Steullet et al. 2017).”
BackgroundAn Update to Calcium Binding Proteins
Elíes, J., Yáñez, M., Pereira, T. D. M. C., Gil‐Longo, J., MacDougall, D. A., & Campos‐Toimil, M. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-12457-1_8 · Cited by 74 · see citing works
Parvalbumin interneuron deficits in schizophrenia
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“Oxidative stress has been reported in many animal models of neurodevelopmental disorders, leading to the suggestion that redox dysregulation might be upstream of PV + interneuron deficits in schizophrenia (Steullet et al., 2017).”
BackgroundThe 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 · see citing works
Astrocytic Regulation of Glutamate Transmission in Schizophrenia
Mei, Y.-Y., Wu, D., & Zhou, N. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00544 · Cited by 64 · see citing works
Parvalbumin interneuron alterations in stress-related mood disorders: A systematic review
Perlman, G., Tanti, A., & Mechawar, N. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100380 · Cited by 65 · see citing works
“, 2013) have higher levels of oxidative stress in the brain, which is negatively associated with the integrity of PV interneurons and their surrounding PNNs (Steullet et al., 2017).”
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“We should investigate in future whether neuropathological changes such as microglial activation in sH-2D-expressing mice are mainly related to MHCI or another molecule expressed and released by astrocytes (Liddelow et al., 2017; Steullet et al., 2017; Yamada et al., 2014).”
BackgroundOpposed hemodynamic responses following increased excitation and parvalbumin-based inhibition
Lee, J., Stile, C. L., Bice, A. R., Rosenthal, Z. P., Yan, P., Snyder, A. Z., Lee, J., & Bauer, A. Q. (2020) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x20930831 · Cited by 51 · see citing works
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Self-citationAssociation of Mitochondrial Biogenesis With Variable Penetrance of Schizophrenia
Li, J., Tran, O., Crowley, T. B., Moore, T. M., Zackai, E. H., Emanuel, B. S., McDonald‐McGinn, D. M., Gur, R. E., Wallace, D. C., & Anderson, S. A. (2021) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2021.0762 · Cited by 61 · see citing works
MicroRNAs in the Onset of Schizophrenia
Thomas, K. T., & Zakharenko, S. S. (2021) · Cells · doi:10.3390/cells10102679 · Cited by 59 · see citing works
“Increased oxidative stress and deficits in PV+ interneurons and PNN labeling have been documented in patients with SCZ [242–246] and in most SCZ mouse models [247].”
BackgroundCanetta, S. E., Holt, E. S., Benoit, L. J., Teboul, E., Sahyoun, G. M., Ogden, R. T., Harris, A. Z., & Kellendonk, C. (2022) · eLife · doi:10.7554/elife.80324 · Cited by 59 · see citing works
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Self-citationThe Role of Serine Racemase in the Pathophysiology of Brain Disorders
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“Steullet et al. (2017) have summarized the evidence that an important pathologic feature of schizophrenia is the downregulation of the presynaptic markers for the cortical fast-firing PV + GABAergic neurons, which provide recurrent inhibition to the pyramidal neurons.”
BackgroundSelf-citationDiurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex
Harkness, J. H., Gonzalez, A. E., Bushana, P. N., Jorgensen, E. T., Hegarty, D. M., Nardo, A. A. D., Prochiantz, A., Wisor, J. P., Aicher, S. A., Brown, T. E., et al. (2021) · Brain Structure and Function · doi:10.1007/s00429-021-02229-4 · Cited by 51 · see citing works
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Brain energy homeostasis: the evolution of the astrocyte-neuron lactate shuttle hypothesis
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Incubation of depression: ECM assembly and parvalbumin interneurons after stress
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Regulation of Reactive Oxygen Species-Mediated Damage in the Pathogenesis of Schizophrenia
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GABAergic System Dysfunction and Challenges in Schizophrenia Research
Jahangir, M., Zhou, J., Lang, B., & Wang, X. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.663854 · Cited by 52 · see citing works
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Thalamic inhibitory circuits and network activity development
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“(Hashemi et al., 2017; Lee et al., 2017; Steullet et al., 2017) PV containing cells are susceptible to oxidative injury and make up the largest subgroup of cortical inhibitory interneurons.”
Western Pacific ALS-PDC: Evidence implicating cycad genotoxins
Spencer, P. S., Palmer, V. S., & Kisby, G. E. (2020) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2020.117185 · Cited by 50 · see citing works
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Behavioral Tasks Evaluating Schizophrenia-like Symptoms in Animal Models: A Recent Update
Ang, M. J., Lee, S., Kim, J.-C., Kim, S., & Moon, C. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200814175114 · Cited by 51 · see citing works
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“This pathoclisis helps explain their putative relationship to abnormalities of gamma aminobutyric acidergic (GABAergic) neurotransmission in many psychiatric disorders [3].”
BackgroundProteoglycan Sulphation in the Function of the Mature Central Nervous System
Fawcett, J. W., & Kwok, J. C. F. (2022) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2022.895493 · Cited by 48 · see citing works
“In mammals, sulphated CSs are produced by the family of carbohydarate sulfotransferases (Chsts) while sulphated HSs are produced by the family of heparan sulfotransferases (Hssts and Ndsts) (Sugahara and Kitagawa, 2000; Esko and Lindahl, 2001).”
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Advancing preclinical models of psychiatric disorders with human brain organoid cultures
Dixon, T. A., & Muotri, A. R. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01708-2 · Cited by 48 · see citing works
“Further incorporating the ‘two-hit’ model would mean a subthreshold immune challenge around adolescence primes microglia activation, causing reactive oxygen species production and specific convergent parvalbumin/perineuronal net dysfunction conserved across psychosis models both of animal and in vitro origin [158].”
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Self-citationCingulate-basal ganglia-thalamo-cortical aspects of catatonia and implications for treatment
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“This is consistent with the notion that redox dysregulation / oxidative stress constitutes a convergent pathological pathway causing PNN / PVI anomalies in many animal models relevant to SZ (Steullet et al., 2017).”
InfluentialSelf-citationForsingdal, A., Jørgensen, T. N., Olsen, L., Werge, T. M., Didriksen, M., & Nielsen, J. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.07.004 · Cited by 40 · see citing works
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“PV-positive neurons are sensitive to oxidative stress (Jiang et al., 2013; Kann et al., 2014; Steullet et al., 2017), and number of PV-positive neurons was reduced in the hippocampus of AD mouse models as well as AD patients (Takahashi et al., 2010).”
BackgroundSantos‐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
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Prevention of schizophrenia deficits via non-invasive adolescent frontal cortex stimulation in rats
Hadar, R., Winter, R. E., Edemann-Callesen, H., Wieske, F., Habelt, B., Khadka, N., Felgel-Farnholz, V., Hlusicka, E. B., Reis, J., Tătărău, C. A., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0356-x · Cited by 38 · see citing works
“Further, since the perceptual alterations as well as social de fi cits in schizophrenia are sought to be related to impaired parvalbumin signaling [32], one could speculate that the lack of effect of tDCS on SI and SC might be a consequence of its inability to affect parvalbumin-cell levels, and…”
Ibrahim, B. A., & Llano, D. A. (2019) · Brain Sciences · doi:10.3390/brainsci9120351 · Cited by 34 · see citing works
“mutations to mimic neurological diseases, such as schizophrenia, cognitive dysfunction, and autism spectrum diseases, were characterized by increasing oxidative stress indicated by high levels of 8-hydroxy-2’-deoxyguanosine immunoreactivity, a marker of DNA oxidative damage, as well as a low percentage of parvalbumin-…”
BackgroundDwir, D., Cabungcal, J.-H., Xin, L., Giangreco, B., Parietti, E., Cleusix, M., Jenni, R., Klauser, P., Conus, P., Cuénod, M., et al. (2021) · Schizophrenia Bulletin · doi:10.1093/schbul/sbab066 · Cited by 40 · see citing works
Self-citationRedox and Immune Signaling in Schizophrenia: New Therapeutic Potential
Dwir, D., Khadimallah, I., Xin, L., Rahman, M., Du, F., Öngür, D., & Kim, Q. (2023) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyad012 · Cited by 40 · see citing works
“These observations converge on OxS-induced PVI/PNN impairment as a “final common pathway” in the pathophysiology of SZ (Steullet et al., 2017).”
BackgroundD’Antoni, C., Mautone, L., Sanchini, C., Tondo, L., Grassmann, G., Cidonio, G., Bezzi, P., Cordella, F., & Angelantonio, S. D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310762 · Cited by 39 · see citing works
Lv, H., Zhu, C., Wu, R., Ni, H., Lian, J., Xu, Y., Xia, Y., Shi, G., Li, Z., Caldwell, R. B., et al. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.04.008 · Cited by 39 · see citing works
A conceptualized model linking matrix metalloproteinase-9 to schizophrenia pathogenesis
Bitanihirwe, B. K. Y., & Woo, T.-U. W. (2020) · Schizophrenia Research · doi:10.1016/j.schres.2019.12.015 · Cited by 34 · see citing works
Sanz‐Morello, B., Pfisterer, U., Hansen, N. W., Demharter, S., Thakur, A., Fujii, K., Левицкий, С. А., Montalant, A., Korshunova, I., Mammen, P. P. A., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2020105759 · Cited by 33 · see citing works
“…showed that Cox6a2 (cid:1) / (cid:1) contributes to hyperactivity, whereas social and acoustic startle behaviors that are often affected in animal models of mental disorders such as schizophrenia (Meechan et al , 2009; Steullet et al , 2017) were not changed in Cox6a2 (cid:1) / (cid:1) mice.”
InfluentialReichelt, A. C., Lemieux, C. A., Princz‐Lebel, O., Singh, A., Bussey, T. J., & Saksida, L. M. (2021) · Scientific Reports · doi:10.1038/s41598-021-85092-x · Cited by 39 · see citing works
Santos‐Silva, T., Colodete, D. A. E., Lisboa, J. R., Freitas, I. D. S., Lopes, C. F. B., Hadera, V., Lima, T. S. A., Souza, A. J., & Gomes, F. V. (2024) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13994 · Cited by 36 · see citing works
- Authors
- Steullet, P., Cabungcal, J.-H., Coyle, J., Didriksen, M., Gill, K., Grace, A. A., Hensch, T. K., LaMantia, A.-S., Lindemann, L., Maynard, T. M., Meyer, U., Morishita, H., O'Donnell, P., Puhl, M., Cuenod, M., & Do, K. Q.
- Affiliations
- Centre Hospitalier Universitaire Vaudois (CH)
- Harvard University (US)
- Lundbeck (Denmark) (DK)
- University of Pittsburgh (US)
- Boston Children's Hospital (US)
- George Washington University (US)
- F. Hoffmann-La Roche AG (CH)
- University of Zurich (CH)
- Corresponding author
- Do, K Q
- ORCID
- Venue
- Molecular Psychiatry
- Published
- 2017-03-21
- Volume
- 22
- Issue
- 7
- Pages
- 936-943
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- PMC
- PMC5491690
- OpenAlex
- W2603460853
- Semantic Scholar
- e687035417ce8207aad80d62600ba2b46fd8efb1
- Cited by
- 360
- References
- 118
- Citations by year
- 2026: 32 · 2025: 28 · 2024: 38 · 2023: 36 · 2022: 44 · 2021: 62 · 2020: 46 · 2019: 34 · 2018: 30 · 2017: 10
- FWCI
- 26.94
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Molecular Psychiatry (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- SERVAL (Université de Lausanne) (publishedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by-nc-nd)
- IRIS (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by-nc-nd)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (125759, 310030_135736/1, 116689, 310030)
- Centre Hospitalier Universitaire Vaudois
- National Institute of Mental Health (P50MH094271, R21MH106919)
- National Eye Institute (R21EY026702, R01EY026053, R01EY024918)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD042182)
- 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 › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- parvalbumin interneurons, oxidative stress, schizophrenia, autism spectrum disorder, anterior cingulate cortex, perineuronal nets, redox dysregulation, antioxidant treatment, glutamatergic signaling, dopaminergic signaling, immune signaling, excitation-inhibition balance, neuronal synchronization, animal models of psychiatric disorders
- MeSH terms
- Autism Spectrum Disorder, Animals, Disease Models, Animal, Gyrus Cinguli, Humans, Interneurons, Oxidation-Reduction, Parvalbumins, Schizophrenia, Oxidative Stress, Mice
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.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-07.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-07.
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.
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