Maternal immune activation leads to selective functional deficits in offspring parvalbumin interneurons

Canetta, S; Bolkan, S; Padilla-Coreano, N; Song, L J; Sahn, R; Harrison, N L; Gordon, J A; Brown, A; Kellendonk, C

doi:10.1038/mp.2015.222

Cited by 201Tryptophan and brain disordersNeuroscience and Neuropharmacology ResearchSchizophrenia research and treatment

Maternal immune activation leads to selective functional deficits in offspring parvalbumin interneurons

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Canetta, S, Bolkan, S, Padilla-Coreano, N, Song, L J, Sahn, R, Harrison, N L, Gordon, J A, Brown, A +1 more·2016·Molecular Psychiatry

DOI 10.1038/mp.2015.222PMC PMC4914410

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Abstract

Abnormalities in prefrontal gamma aminobutyric acid (GABA)ergic transmission, particularly in fast-spiking interneurons that express parvalbumin (PV), are hypothesized to contribute to the pathophysiology of multiple psychiatric disorders, including schizophrenia, bipolar disorder, anxiety disorders and depression. While primarily histological abnormalities have been observed in patients and in animal models of psychiatric disease, evidence for abnormalities in functional neurotransmission at the level of specific interneuron populations has been lacking in animal models and is difficult to establish in human patients. Using an animal model of a psychiatric disease risk factor, prenatal maternal immune activation (MIA), we found reduced functional GABAergic transmission in the medial prefrontal cortex (mPFC) of adult MIA offspring. Decreased transmission was selective for interneurons expressing PV, resulted from a decrease in release probability and was not observed in calretinin-expressing neurons. This deficit in PV function in MIA offspring was associated with increased anxiety-like behavior and impairments in attentional set shifting, but did not affect working memory. Furthermore, cell-type specific optogenetic inhibition of mPFC PV interneurons was sufficient to impair attentional set shifting and enhance anxiety levels. Finally, we found that in vivo mPFC gamma oscillations, which are supported by PV interneuron function, were linearly correlated with the degree of anxiety displayed in adult mice, and that this correlation was disrupted in MIA offspring. These results demonstrate a selective functional vulnerability of PV interneurons to MIA, leading to affective and cognitive symptoms that have high relevance for schizophrenia and other psychiatric disorders.

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Several prenatal factors, such as immune and endocrine systems, strongly affect postnatal network trajectories.
“It is also clear that several prenatal factors (e.g. immune and endocrine systems) strongly affect postnatal network trajectories (Canetta et al., 2016; Scheinost et al., 2016b).”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Canetta et al., 2016

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Maternal immune activation: Implications for neuropsychiatric disorders
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Generation of a microglial developmental index in mice and in humans reveals a sex difference in maturation and immune reactivity
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Plastic and neuroprotective mechanisms involved in the therapeutic effects of cannabidiol in psychiatric disorders
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The Interaction between the Immune System and Epigenetics in the Etiology of Autism Spectrum Disorders
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Early Life Stress Drives Sex-Selective Impairment in Reversal Learning by Affecting Parvalbumin Interneurons in Orbitofrontal Cortex of Mice
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The Number of Chandelier and Basket Cells Are Differentially Decreased in Prefrontal Cortex in Autism
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Advantages and Limitations of Animal Schizophrenia Models
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Cross-hemispheric gamma synchrony between prefrontal parvalbumin interneurons supports behavioral adaptation during rule shift learning
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Maternal inflammation has a profound effect on cortical interneuron development in a stage and subtype-specific manner
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Maternal inhalation of carbon black nanoparticles induces neurodevelopmental changes in mouse offspring
Umezawa, M., Onoda, A., Korshunova, I., Jensen, A. C. Ø., Koponen, I. K., Jensen, K. A., Khodosevich, K., Vogel, U. B., & Hougaard, K. S. (2018) · Particle and Fibre Toxicology · doi:10.1186/s12989-018-0272-2 · Cited by 86 · see citing works
Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human
Stolp, H. B., Fleiss, B., Arai, Y., Supramaniam, V., Vontell, R., Birtles, S., Yates, A. G., Baburamani, A. A., Thornton, C., Rutherford, M., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00955 · Cited by 85 · see citing works
Maternal and Early Postnatal Immune Activation Produce Dissociable Effects on Neurotransmission in mPFC–Amygdala Circuits
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Maternal immune activation and role of placenta in the prenatal programming of neurodevelopmental disorders
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Developmental disruption of perineuronal nets in the medial prefrontal cortex after maternal immune activation
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Two opposing hippocampus to prefrontal cortex pathways for the control of approach and avoidance behaviour
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Cholecystokinin-Expressing Interneurons of the Medial Prefrontal Cortex Mediate Working Memory Retrieval
Nguyen, R., Venkatesan, S., Binko, M. A., Bang, J. Y., Cajanding, J. D., Briggs, C., Sargin, D., Imayoshi, I., Lambe, E. K., & Kim, J. C. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1919-19.2020 · Cited by 72 · see citing works
The role of microglia in early neurodevelopment and the effects of maternal immune activation
Mastenbroek, L., Kooistra, S. M., Eggen, B. J. L., & Prins, J. R. (2024) · Seminars in Immunopathology · doi:10.1007/s00281-024-01017-6 · Cited by 77 · see citing works
The Nature of Prefrontal Cortical GABA Neuron Alterations in Schizophrenia: Markedly Lower Somatostatin and Parvalbumin Gene Expression Without Missing Neurons
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Role of the innate immune system in the neuropathological consequences induced by adolescent binge drinking
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The Fragile Brain: Stress Vulnerability, Negative Affect and GABAergic Neurocircuits in Psychosis
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Paliperidone reverts Toll-like receptor 3 signaling pathway activation and cognitive deficits in a maternal immune activation mouse model of schizophrenia
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Adolescent thalamic inhibition leads to long-lasting impairments in prefrontal cortex function
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Sex Differences in Neurodevelopmental Disorders: A Key Role for the Immune System
Breach, M. R., & Lenz, K. M. (2022) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2022_308 · Cited by 62 · see citing works
Biphasic Impact of Prenatal Inflammation and Macrophage Depletion on the Wiring of Neocortical Inhibitory Circuits
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Elevated expression of complement C4 in the mouse prefrontal cortex causes schizophrenia-associated phenotypes
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Maternal immune activation alters fetal and neonatal microglia phenotype and disrupts neurogenesis in mice
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Mature parvalbumin interneuron function in prefrontal cortex requires activity during a postnatal sensitive period
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Effects of the mode of re-socialization after juvenile social isolation on medial prefrontal cortex myelination and function
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Maternal immune activation impairs cognitive flexibility and alters transcription in frontal cortex
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Microglial GPR56 is the molecular target of maternal immune activation-induced parvalbumin-positive interneuron deficits
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At the crux of maternal immune activation: Viruses, microglia, microbes, and IL‐17A
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Prenatal maternal immune activation and brain development with relevance to psychiatric disorders
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Male fetus susceptibility to maternal inflammation: C-reactive protein and brain development
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Long-range inhibition synchronizes and updates prefrontal task activity
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AutDB: a platform to decode the genetic architecture of autism
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Effects of early or late prenatal immune activation in mice on behavioral and neuroanatomical abnormalities relevant to schizophrenia in the adulthood
da Silveira, V. T., de Castro Medeiros, D., Ropke, J., Guidine, P. A., Rezende, G. H., Moraes, M. F. D., Mendes, E. M. A. M., Macedo, D., Moreira, F. A., & de Oliveira, A. C. P. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.01.009 · Cited by 51 · see citing works
Modulating microglia activation prevents maternal immune activation induced schizophrenia-relevant behavior phenotypes via arginase 1 in the dentate gyrus
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Step by step: cells with multiple functions in cortical circuit assembly
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The iPSC perspective on schizophrenia
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Cortical Gray Matter Injury in Encephalopathy of Prematurity: Link to Neurodevelopmental Disorders
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Microglia and Sensitive Periods in Brain Development
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Prefrontal and Hippocampal Parvalbumin Interneurons in Animal Models for Schizophrenia: A Systematic Review and Meta-analysis
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The GABA Developmental Shift Is Abolished by Maternal Immune Activation Already at Birth
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Redox 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
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Authors: Canetta, S., Bolkan, S., Padilla-Coreano, N., Song, L. J., Sahn, R., Harrison, N. L., Gordon, J. A., Brown, A., & Kellendonk, C.
Affiliations: Columbia University Irving Medical Center (US)
Corresponding author: Kellendonk, C
ORCID: Canetta, S
Padilla-Coreano, N
Song, L J
Harrison, N L
Gordon, J A
Brown, A
Kellendonk, C
Venue: Molecular Psychiatry
Publisher: Springer Science and Business Media LLC
Published: 2016-02-02
Volume: 21
Issue: 7
Pages: 956-968
ISSN: 1359-4184 (ISSN-L)
1476-5578
DOI: 10.1038/mp.2015.222
PMC: PMC4914410
OpenAlex: W2258502568
Cited by: 201
References: 98
Citations by year: 2026: 11 · 2025: 21 · 2024: 14 · 2023: 25 · 2022: 28 · 2021: 24 · 2020: 20 · 2019: 17 · 2018: 15 · 2017: 15 · 2016: 11
FWCI: 6.43
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Molecular Psychiatry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Alcohol Abuse and Alcoholism (R01AA019801, R01AA023531)
National Institute of Mental Health (T32MH016434, K02MH065422, K01MH107760)
National Cancer Institute (P30CA013696)
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Keywords: maternal immune activation, parvalbumin interneurons, GABAergic neurotransmission, medial prefrontal cortex, release probability, anxiety-like behavior, set-shifting, working memory, optogenetic inhibition, gamma oscillations, schizophrenia, mental illness, calretinin interneurons, prenatal immune activation
MeSH terms: Animals, Disease Models, Animal, Female, gamma-Aminobutyric Acid, Humans, Immunity, Active, Inhibition, Psychological, Interneurons, Male, Memory, Short-Term, Synaptic Transmission, Parvalbumins, Pregnancy, Prenatal Exposure Delayed Effects, Prefrontal Cortex, Mice, GABAergic Neurons

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Maternal immune activation leads to selective functional deficits in offspring parvalbumin interneurons

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