Activation of the Maternal Immune System During Pregnancy Alters Behavioral Development of Rhesus Monkey Offspring
Open accessAbstract
Background Maternal infection during pregnancy is associated with an increased risk of schizophrenia and autism in the offspring. Supporting this correlation, experimentally activating the maternal immune system during pregnancy in rodents produces offspring with abnormal brain and behavioral development. We have developed a nonhuman primate model to bridge the gap between clinical populations and rodent models of maternal immune activation (MIA).Methods A modified form of the viral mimic, synthetic double-stranded RNA (polyinosinic:polycytidylic acid stabilized with poly-L-lysine) was delivered to two separate groups of pregnant rhesus monkeys to induce MIA: 1) late first trimester MIA (n = 6), and 2) late second trimester MIA (n = 7). Control animals (n = 11) received saline injections at the same first or second trimester time points or were untreated. Sickness behavior, temperature, and cytokine profiles of the pregnant monkeys confirmed a strong inflammatory response to MIA.Results Behavioral development of the offspring was studied for 24 months. Following weaning at 6 months of age, MIA offspring exhibited abnormal responses to separation from their mothers. As the animals matured, MIA offspring displayed increased repetitive behaviors and decreased affiliative vocalizations. When evaluated with unfamiliar conspecifics, first trimester MIA offspring deviated from species-typical macaque social behavior by inappropriately approaching and remaining in immediate proximity of an unfamiliar animal.Conclusions In this rhesus monkey model, MIA yields offspring with abnormal repetitive behaviors, communication, and social interactions. These results extended the findings in rodent MIA models to more human-like behaviors resembling those in both autism and schizophrenia.
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Maternal immune activation is associated with ASD risk.
“While mounting evidence points to the role of maternal immune activation in ASD risk,”
From The contribution of environmental exposure to the etiology of autism spectrum disorder (2019) · cites this paper as [105]
Mouse MIA offspring show localized aberrations in Purkinje cells, similar to the localized deficits in cerebellar Purkinje cells that have been reported in many postmortem ASD cases.
“mouse MIA offspring show localized aberrations in Purkinje cells98, similar to the localized deficits in cerebellar Purkinje cells that have been reported in many postmortem ASD cases99.”
From Immune mediators in the brain and peripheral tissues in autism spectrum disorder (2015) · cites this paper as [98]
Bauman et al. extended the poly(I:C) maternal activation model to rhesus macaques and found abnormal vocal communication, social interaction, and repetitive behaviors in the offspring.
“A 2014 study by Bauman et al (2014), broadened the poly (I:C) maternal activation model to rhesus macaques, showing many abnormal behaviors, including in vocal communication and social interaction, as well as repetitive behaviors in the offspring of treated females.”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Bauman et al, 2014
Similarities between autism and schizophrenia are such that results from animal models like the MIA model may be overlapping and confounded.
“Despite the differences between these two disorders, the similarities between them are such that results from animal models like the MIA model may be overlapping and confounded (Bauman et al, 2014;Young et al, 2016).”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Bauman et al, 2014
Schizophrenia and autism share many immune similarities, including a subset of patients with an etiology based in maternal infection and immune activation.
“Schizophrenia and autism share many immune similarities, including a subset of patients with an etiology based in maternal infection and immune activation (Bauman et al, 2014;Boksa, 2010;Brown et al, 2004a;Meyer et al, 2005Meyer et al, , 2007;;Patterson, 2009;Urakubo et al, 2001).”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Bauman et al, 2014
Mice and/or non-human primates exposed to maternal immune activation through maternal infection with poly(I:C) or maternal influenza infection have offspring that develop abnormal social behaviors, deficits in immune profiles and anxiety-like phenotypes.
“Similarly, mice and/or non-human primates that are exposed to maternal immune activation (MIA) through maternal infection with the viral mimetic, polyinosinic: polycitidylic acid (poly (I:C)), or maternal influenza infection, have offspring that develop abnormal social behaviors 646566, deficits in their immune profiles and anxiety-like phenotypes 67.”
From Gastrointestinal Issues and Autism Spectrum Disorder (2020) · cites this paper as [65]
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- Authors
- Bauman, M. D., Iosif, A.-M., Smith, S. E. P., Bregere, C., Amaral, D. G., & Patterson, P. H.
- Affiliations
- University of California, Davis (US)
- California Institute of Technology (US)
- Corresponding author
- Bauman, Melissa D.
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2014-02
- Volume
- 75
- Issue
- 4
- Pages
- 332-341
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC6782053
- OpenAlex
- W2119799034
- Cited by
- 294
- References
- 120
- Citations by year
- 2026: 10 · 2025: 13 · 2024: 19 · 2023: 13 · 2022: 34 · 2021: 25 · 2020: 26 · 2019: 25 · 2018: 27 · 2017: 28 · 2016: 26 · 2015: 29 · 2014: 17 · 2013: 1
- FWCI
- 8.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Simons Foundation Autism Research Initiative (9900060, RR00169)
- Office of Research Infrastructure Programs, National Institutes of Health
- Simons Foundation
- National Center for Research Resources (R24RR019970, P51RR000169)
- California National Primate Research Center
- Office of the Director (P51OD011157, R24OD010962)
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Keywords
- maternal immune activation, rhesus monkeys, prenatal immune activation, schizophrenia, autism spectrum disorder, repetitive behavior, social behavior, maternal separation, social novelty, nonhuman primate model, cytokines, sickness behavior, polyinosinic-polycytidylic acid
- MeSH terms
- Animals, Behavior, Animal, Mental Disorders, Brain, Carboxymethylcellulose Sodium, Disease Models, Animal, Female, Macaca mulatta, Maternal Deprivation, Poly I-C, Polylysine, Pregnancy, Pregnancy Complications, Infectious, Prenatal Exposure Delayed Effects, Social Behavior, Stereotyped Behavior, Vocalization, Animal, Maternal Exposure
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