Sex-specific disruptions in spatial memory and anhedonia in a “two hit” rat model correspond with alterations in hippocampal brain-derived neurotrophic factor expression and signaling
Abstract
Post-mortem studies have demonstrated reduced expression of brain-derived neurotrophic factor (BDNF) in the hippocampus of schizophrenia and major depression patients. The "two hit" hypothesis proposes that two or more major disruptions at specific time points during development are involved in the pathophysiology of these mental illnesses. However, the role of BDNF in these "two hit" effects is unclear. Our aim was to behaviorally characterize a "two hit" rat model of developmental stress accompanied by an in-depth assessment of BDNF expression and signalling. Wistar rats were exposed to neonatal maternal separation (MS) stress and/or adolescent/young-adult corticosterone (CORT) treatment. In adulthood, models of cognitive and negative symptoms of mental illness were analyzed. The hippocampus was then dissected into dorsal (DHP) and ventral (VHP) regions and analyzed by qPCR for exon-specific BDNF gene expression or by Western blot for BDNF protein expression and downstream signaling. Male "two hit" rats showed marked disruptions in short-term spatial memory (Y-maze) which were absent in females. However, female "two hit" rats showed signs of anhedonia (sucrose preference test), which were absent in males. Novel object recognition and anxiety (elevated plus maze) were unchanged by either of the two "hits". In the DHP, MS caused a male-specific increase in BDNF Exons I, II, IV, VII, and IX mRNA but a decrease in mature BDNF and phosphorylated TrkB (pTrkB) protein expression in adulthood. In the VHP, BDNF transcript expression was unchanged; however, in female rats only, MS significantly decreased mature BDNF and pTrkB protein expression in adulthood. These data demonstrate that MS causes region-specific and sex-specific long-term effects on BDNF expression and signaling and, importantly, mRNA expression does not always infer protein expression. Alterations to BDNF signaling may mediate the sex-specific effects of developmental stress on anhedonic behaviors.
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Several studies found that maternal separation alone did not change sucrose preference, but a second stressor in adolescence or adulthood reduced sucrose preference.
“Several studies found that while maternal separation by itself did not result in changes in sucrose preference, occurrence of a second stressor or challenge in adolescence or adulthood resulted in reduced sucrose preference (Hill et al., 2014; Klug and van den Buuse, 2012; Uchida et al., 2010).”
From The effects of early life stress on reward processing (2018) · cites this paper as Hill et al., 2014
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“Several studies found that while maternal separation by itself did not result in changes in sucrose preference, occurrence of a second stressor or challenge in adolescence or adulthood resulted in reduced sucrose preference (Hill et al., 2014; Klug and van den Buuse, 2012; Uchida et al., 2010).”
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Ρυακιωτάκης, Ε., Fousfouka, D., & Stamatakis, A. (2026) · Neuroscience · doi:10.1016/j.neuroscience.2026.10.003
- Authors
- Hill, R. A., Klug, M., Kiss Von Soly, S., Binder, M. D., Hannan, A. J., & van den Buuse, M.
- Affiliations
- The University of Melbourne (AU)
- Florey Institute of Neuroscience and Mental Health, University of Melbourne Parkville Victoria Australia
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2014-05-16
- Volume
- 24
- Issue
- 10
- Pages
- 1197-1211
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W1485846260
- Cited by
- 99
- References
- 85
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 5 · 2023: 7 · 2022: 7 · 2021: 14 · 2020: 5 · 2019: 10 · 2018: 8 · 2017: 7 · 2016: 14 · 2015: 13 · 2014: 3
- FWCI
- 5.63
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NHMRC (566879)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Keywords
- brain-derived neurotrophic factor, BDNF signaling, TrkB phosphorylation, two-hit hypothesis, developmental stress, neonatal maternal separation, corticosterone, sex differences, dorsal hippocampus, ventral hippocampus, spatial memory, anhedonia, schizophrenia, major depressive disorder, negative symptoms
- MeSH terms
- Animals, Anxiety, Corticosterone, Disease Models, Animal, Feeding Behavior, Female, Hippocampus, Male, Maternal Deprivation, Memory Disorders, Memory, Short-Term, Random Allocation, RNA, Messenger, Sex Characteristics, Stress, Psychological, Rats, Wistar, Brain-Derived Neurotrophic Factor, Dietary Sucrose, Receptor, trkB, Recognition, Psychology, Taste Perception, Anhedonia, Spatial Memory
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