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Early life stress disrupts social behavior and prefrontal cortex parvalbumin interneurons at an earlier time-point in females than in males
Open accessAbstract
Early life stress exposure (ELS) yields risk for psychiatric disorders that might occur though a population-specific mechanism that impacts prefrontal cortical development. Sex differences in ELS effects are largely unknown and are also essential to understand social and cognitive development. ELS can cause dysfunction within parvalbumin (PVB)-containing inhibitory interneurons in the prefrontal cortex and in several prefrontal cortex-mediated behaviors including social interaction. Social behavior deficits are often the earliest observed changes in psychiatric disorders, therefore the time-course and causation of social interaction deficits after ELS are important to determine. PVB interneuron dysfunction can disrupt social behavior, and has been correlated in males with elevated markers of oxidative stress and inflammation, such as cyclooxygenase-2 after ELS. Here, we measured the effects of maternal separation ELS on social interaction behaviors in males and females. Prefrontal cortex PVB and cyclooxygenase-2 were also measured in juveniles and adolescents using Western blots. ELS led to social interaction alterations earlier in females than males. Sexually dimorphic behavioral changes were consistent with prefrontal cortex PVB loss after ELS. PVB levels were decreased in ELS-exposed juvenile females, while males exposed to ELS do not display parvalbumin decreases until adolescence. Early behavioral and PVB changes in females did not appear to be mediated through cyclooxygenase-2, since levels were not affected in ELS females. Therefore, these data suggest that ELS affects males and females differently and with distinct developmental profiles.
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“The reduction in PV+ interneuron densities we observed in the MSEW hippocampus is likely due to decreased PV protein levels rather than loss of neurons given our data on PV expression and GAD67+ cell densities, as well as previous studies showing reductions in PV protein levels due to early life adversity in the mPFC of juvenile mice (68; 69).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [69]
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Neocortical excitation/inhibition balance in information processing and social dysfunction
Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O’Shea, D. J., Sohal, V. S., Goshen, I., Finkelstein, J., Paz, J. T., et al. (2011) · Nature · doi:10.1038/nature10360 · Cited by 2,454
Sex bias in neuroscience and biomedical research
Beery, A. K., & Zucker, I. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.07.002 · Cited by 1,763
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638
Shank3 mutant mice display autistic-like behaviours and striatal dysfunction
Peça, J., Feliciano, C., Ting, J. T., Wang, W., Wells, M. F., Venkatraman, T. N., Lascola, C. D., Fu, Z., & Feng, G. (2011) · Nature · doi:10.1038/nature09965 · Cited by 1,570
Trajectories of brain development: point of vulnerability or window of opportunity?
Andersen, S. L. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00005-8 · Cited by 1,503
The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course
McEwen, B. S., & Morrison, J. H. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.028 · Cited by 1,079
Peñagarikano, O., Abrahams, B. S., Herman, E. I., Winden, K. D., Gdalyahu, A., Dong, H., Sonnenblick, L. I., Gruver, R., Almajano, J., Bragin, A., et al. (2011) · Cell · doi:10.1016/j.cell.2011.08.040 · Cited by 1,075
Insel, T. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.005 · Cited by 1,044
Infantile Experience and Resistance to Physiological Stress
Levine, S. (1957) · Science · doi:10.1126/science.126.3270.405 · Cited by 659
Read, J., Perry, B. D., Moskowitz, A., & Connolly, J. (2001) · Psychiatry: Interpersonal and Biological Processes · doi:10.1521/psyc.64.4.319.18602 · Cited by 594
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Geloso, M. C., Sante, G. D., & Granato, A. (2026) · Cells · doi:10.3390/cells15100869 · Cited by 1
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Santos‐Silva, T., Godoy, L. D., Guimarães, F. S., & Gomes, F. V. (2026) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyag043 · Cited by 1
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Echeverry, M. B., Takada, S. H., Arruda, B. P., Cardoso, D. S., Martins, P. P., Ikebara, J. M., Santos, A. V. S., & Silva, V. R. C. T. D. (2021) · IntechOpen eBooks · doi:10.5772/intechopen.100055 · Cited by 1
Sun Metro Fixed Route Rider Survey
Soden, D. L., McElroy, M., & Green, S. (2006) · scholarworks - UTEP (The University of Texas at El Paso) · Cited by 1
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Rekapalli, A. K., Roman, I. C., Brenhouse, H. C., & Cody, C. R. (2024) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10367 · Cited by 1
Hall, S., Hawkins, K., Laws, G. C., Akitt, T., Simon, A., Davies, C. H., Whittington, M. A., & Cunningham, M. O. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/298612
Díaz, C. G. (2021) · Tesis Doctorals en Xarxa (Consorci de Serveis Universitaris de Catalunya) · doi:10.6035/14112.2021.403202
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Bonauto, S. M., Wilson, P. L., & Honeycutt, J. A. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5387627
Campbell, T. S., Skweres, A., Jose, A., & Roth, T. L. (2025) · Brain and Environment · doi:10.1016/j.braen.2025.100005
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Lynch, A., Brenhouse, H. C., & Breton, J. (2026) · Hormones and Behavior · doi:10.1016/j.yhbeh.2026.105902 · Cited by 1
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Bonauto, S. M., Wilson, P. L., & Honeycutt, J. A. (2026) · Behavioural Brain Research · doi:10.1016/j.bbr.2026.116272
Li, Z., Si, T., Wu, Q.-R., Zhao, J.-H., Hua, W.-Z., Zhang, Y., Yang, S., Mao, Y.-Y., Zang, W., & Cao, J. (2026) · iScience · doi:10.1016/j.isci.2026.116454
Nashawi, H., Foltz, C. T., Oh, N., Santiago, E. A., Selm, D. R., Herman, J. P., & Ulrich‐Lai, Y. M. (2026) · Brain Structure and Function · doi:10.1007/s00429-026-03141-5
Bersotti, F. M., Alves, G., Generoso, V. A., Neiva, G. S., Soares, L. L., Nunes, G. S., Daghastanli, N. A., Prates, I. T. K., & Takada, S. H. (2026) · Neuroscience · doi:10.1016/j.neuroscience.2026.09.014
Metadata
- Authors
- Holland, F. H., Ganguly, P., Potter, D. N., Chartoff, E. H., & Brenhouse, H. C.
- Affiliations
- Northeastern University (US)
- McLean Hospital (US)
- Corresponding author
- Brenhouse, Heather C.
- Venue
- Neuroscience Letters
- Publisher
- Elsevier BV
- Published
- 2014-04
- Volume
- 566
- Pages
- 131-136
- ISSN
- 0304-3940 (ISSN-L)
- PMC
- PMC4476267
- OpenAlex
- W2023467429
- Cited by
- 125
- References
- 39
- Citations by year
- 2026: 13 · 2025: 9 · 2024: 8 · 2023: 10 · 2022: 8 · 2021: 21 · 2020: 14 · 2019: 11 · 2018: 15 · 2017: 2 · 2016: 6 · 2015: 6 · 2014: 1
- FWCI
- 2.45
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuroscience Letters (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R21MH097182)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Keywords
- early life stress, maternal separation, sex differences, social behavior, social interaction deficits, parvalbumin interneurons, prefrontal cortex, cyclooxygenase-2, oxidative stress, inflammation, juvenile development, adolescent development, mental illness
- MeSH terms
- Animals, Female, Interneurons, Male, Maternal Deprivation, Motor Activity, Parvalbumins, Sex Factors, Social Behavior, Stress, Psychological, Rats, Sprague-Dawley, Prefrontal Cortex, Cyclooxygenase 2
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