Voluntary exercise followed by chronic stress strikingly increases mature adult-born hippocampal neurons and prevents stress-induced deficits in’ what-when-where’ memory

Castilla-Ortega, Estela; Rosell-Valle, Cristina; Pedraza, Carmen; Rodríguez de Fonseca, Fernando; Estivill-Torrús, Guillermo; Santín, Luis J.

doi:10.1016/j.nlm.2013.12.001

Cited by 41Neurogenesis and neuroplasticity mechanismsMemory and Neural MechanismsStress Responses and Cortisol

Voluntary exercise followed by chronic stress strikingly increases mature adult-born hippocampal neurons and prevents stress-induced deficits in’ what-when-where’ memory

Castilla-Ortega, Estela, Rosell-Valle, Cristina, Pedraza, Carmen, Rodríguez de Fonseca, Fernando, Estivill-Torrús, Guillermo, Santín, Luis J.·2014·Neurobiology of Learning and Memory

DOI 10.1016/j.nlm.2013.12.001

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Abstract

We investigated whether voluntary exercise prevents the deleterious effects of chronic stress on episodic-like memory and adult hippocampal neurogenesis. After bromodeoxyuridine (BrdU) administration, mice were assigned to receive standard housing, chronic intermittent restraint stress, voluntary exercise or a combination of both (stress starting on the seventh day of exercise). Twenty-four days later, mice were tested in a 'what-when-where' object recognition memory task. Adult hippocampal neurogenesis (proliferation, differentiation, survival and apoptosis) and c-Fos expression in the hippocampus and extra-hippocampal areas (medial prefrontal cortex, amygdala, paraventricular hypothalamic nucleus, accumbens and perirhinal cortex) were assessed after behavior. Chronic intermittent restraint stress impaired neurogenesis and the 'when' memory, while exercise promoted neurogenesis and improved the 'where' memory. The 'when' and 'where' memories correlated with c-Fos expression in CA1 and the dentate gyrus, respectively. Furthermore, analysis suggested that each treatment induced a distinct pattern of functional connectivity among the areas analyzed for c-Fos. In the animals in which stress and exercise were combined, stress notably reduced the amount of voluntary exercise performed. Nevertheless, exercise still improved memory and counteracted the stress induced-deficits in neurogenesis and behavior. Interestingly, compared with the other three treatments, the stressed exercising animals showed a larger increase in cell survival, the maturation of new neurons and apoptosis in the dentate gyrus, with a considerable increase in the number of 24-day-old BrdU+cells that differentiated into mature neurons. The interaction between exercise and stress in enhancing the number of adult-born hippocampal neurons supports a role of exercise-induced neurogenesis in stressful conditions.

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The replicability of the ELM2-2 and ELM2-1 tests is verified by independent laboratories.
“The replicability of the ELM2–2 and ELM2–1 tests is verified by independent laboratories (Barbosa et al., 2013; Castilla-Ortega et al., 2012; Castilla-Ortega et al., 2014; Drieskens et al., 2017; Fernandez and Garner, 2008; Inostroza et al., 2013a; Inostroza et al., 2013b; Lanté et al., 2015; Li and Chao, 2008; Lopez-Pigozzi et al., 2016; Wang et al., 2010).”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Castilla-Ortega et al., 2014
In the ELM2-1 test, c-fos expression in hippocampal CA1 and dentate gyrus required for episodic-like memory was correlated with the when and where components, respectively.
“the c-fos expression of hippocampal CA1 and dentate gyrus required for episodic-like memory was correlated with the when and where components, respectively”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Castilla-Ortega et al., 2014
Voluntary exercise improved neurogenesis and the where index of the ELM2-1 test.
“exercise improved it and the where index of the ELM2–1 test”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Castilla-Ortega et al., 2014
Chronic restraint stress disrupted neurogenesis and the when component.
“restraint disrupted neurogenesis and the when component”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Castilla-Ortega et al., 2014

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Authors: Castilla-Ortega, E., Rosell-Valle, C., Pedraza, C., Rodríguez de Fonseca, F., Estivill-Torrús, G., & Santín, L. J.
Affiliations: Instituto de Investigación Biomédica de Málaga (ES)
Corresponding author: Santín, Luis J.
ORCID: Rosell-Valle, Cristina
Pedraza, Carmen
Santín, Luis J.
Venue: Neurobiology of Learning and Memory
Publisher: Elsevier BV
Published: 2014-03
Volume: 109
Pages: 62-73
ISSN: 1074-7427 (ISSN-L)
DOI: 10.1016/j.nlm.2013.12.001
OpenAlex: W2064758288
Cited by: 41
References: 72
Citations by year: 2026: 1 · 2025: 1 · 2024: 2 · 2023: 6 · 2022: 5 · 2020: 4 · 2019: 3 · 2018: 3 · 2017: 3 · 2016: 3 · 2015: 7 · 2014: 3
FWCI: 1.59
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neurobiology of Learning and Memory (publishedVersion)
PubMed (publishedVersion)
Funders: Universidad de Málaga
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: voluntary exercise, chronic stress, adult hippocampal neurogenesis, episodic-like memory, object recognition memory, Fos expression, dentate gyrus, CA1, neuronal apoptosis, cell survival, neurogenesis, restraint stress, hippocampal functional connectivity
MeSH terms: Animals, Chronic Disease, Hippocampus, Male, Mice, Inbred C57BL, Motor Activity, Neurons, Restraint, Physical, Stress, Psychological, Recognition, Psychology, Mice, Neurogenesis

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Voluntary exercise followed by chronic stress strikingly increases mature adult-born hippocampal neurons and prevents stress-induced deficits in’ what-when-where’ memory

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