Hypoxia and fluoxetine in newborn female rats increase the performance of spatial long-term memory and reactivity of the hypothalamic-pituitary-adrenocortical system in adulthood
DOI:
https://doi.org/10.33910/2687-1270-2023-4-1-79-90Keywords:
neonatal hypoxia and fluoxetine, spatial learning, memory, corticosterone, adult ratAbstract
The study investigated the effects of 1) acute normobaric hypoxia with a reduced oxygen concentration in inhaled air and 2) the selective serotonin reuptake inhibitor fluoxetine in newborn female rat pups on spatial learning, the performance of spatial short-term and long-term memory and reactivity of the hypothalamic-pituitary-adrenal axis (the HPA axis) in adult rats. The newly obtained data indicate a deterioration in the ability for spatial learning only in the first out of five training days. Hypoxia did not change the performance of memory in the test “recognition of a new object” and caused an improvement in long-term memory in the Morris water maze. This was combined with a higher content of corticosterone in blood plasma after testing long-term memory. Fluoxetine did not change the performance indicators of memory or hormonal indicators in either control or hypoxic adult rats. Fluoxetine normalized the latent period of reaching the platform in hypoxic rats when testing learning, and did not reduce the indicator of long-term memory improved by hypoxia. The obtained results suggest that neonatal normobaric hypoxia under certain conditions helps improving memory, while fluoxetine has a protective effect on cognitive abilities and the HPA axis in adult female rats.
References
Alizadeh-Ezdini, Z., Vatanparast, J. (2022) Differential impact of two paradigms of early-life adversity on behavioural responses to social defeat in young adult rats and morphology of CA3 pyramidal neurons. Behavior Brain Research, vol. 435, article 114048. https://doi.org/10.1016/j.bbr.2022.114048 (In English)
Azmitia, E. C. (2001) Modern views on an ancient chemical: Serotonin effects on cell proliferation, maturation, and apoptosis. Brain Research Bulletin, vol. 56, no. 5, pp. 413–424. https://doi.org/10.1016/S0361-9230(01)00614-1 (In English)
Bombardi, C., Grandis, A., Pivac, N. et al. (2021) Serotonin modulation of hippocampal functions: From anatomy to neurotherapeutics. Progress in Brain Research, vol. 261, pp. 83–158. https://doi.org/10.1016/bs.pbr.2021.01.031 (In English)
Bond, A. M., Ming, G-L., Song, H. (2022) What is the relationship between hippocampal neurogenesis across different stages of the lifespan? Frontiers in Neuroscience, vol. 16, article 891713. https://doi.org/10.3389/fnins.2022.891713 (In English)
Brummelte, S., Glanaghy, E., Bonnin, A., Oberlander, T. F. (2017) Developmental changes in serotonin signaling: Implications for early brain function, behavior and adaptation. Neuroscience, vol. 342, no. 7, pp. 212–231. https://doi.org/10.1016/j.neuroscience.2016.02.037 (In English)
Butkevich, I. P., Mikhailenko, V. A. (2018) Effect of fluoxetine in prenatal period on nociceptive system reactivity and psychoemotional behavior in young female rats. Bulletin of Experimental Biology and Medicine, vol. 165, no. 2, pp. 209–212. https://doi.org/10.1007/s10517-018-4131-9 (In English)
Carneiro, I. B. C., Toscano, A. E., da Cunha, M. de S. B. et al. (2022) Serotonergic mechanisms associated with experimental models of hypoxia: A systematic review. International Journal of Developmental Neuroscience, vol. 82, no. 8, pp. 667–679. https://doi.org/10.1002/jdn.10226 (In English)
Casolini, P., Zuena, A. R., Cinque, C. et al. (2005) Sub-neurotoxic neonatal anoxia induces subtle behavioural changes and specific abnormalities in brain group-I metabotropic glutamate receptors in rats. Journal of Neurochemistry, vol. 95, no. 1, pp. 137–145. https://doi.org/10.1111/j.1471-4159.2005.03349.x (In English)
Cohen, S. J., Stackman, R. W. Jr. (2015) Assessing rodent hippocampal involvement in the novel object recognition task. A review. Behavioral Brain Research, vol. 285, pp. 105–117. https://doi.org/10.1016/j.bbr.2014.08.002 (In English) De Gregorio, R., Subah, G., Chan, J. C. et al. (2022) Sex-biased effects on hippocampal circuit development by perinatal SERT expression in CA3 pyramidal neurons. Development, vol. 149, no. 21, article dev200549. https://doi.org/10.1242/dev.200549 (In English)
Dobbing, J. (1981) Nutritional growth restriction and the nervous system. In: A. N. Davidson, R. H. S. Thompson (eds.). The molecular basis of neuropathology. London: Edward Arnold & Co. Publ., pp. 221–233. (In English)
Duran-Carabali, L. E., Odorcyk, F. K., Sanches, E. F. et al. (2022) Effect of environmental enrichment on behavioral and morphological outcomes following neonatal hypoxia-ischemia in rodent models: A systematic review and meta-analysis affiliations expand. Molecular Neurobiology, vol. 59, no. 3, pp. 1970–1991. https://doi.org/10.1007/s12035-022-02730-9 (In English)
Edinoff, A. N., Akuly, H. A., Hanna, T. A. et al. (2021) Selective serotonin reuptake inhibitors and adverse effects: A narrative review. Neurology International, vol. 13, no. 3, pp. 387–401. https://doi.org/10.3390/neurolint13030038 (In English)
France, G., Volianskis, R., Ingram, R. et al. (2022) Differential regulation of STP, LTP and LTD by structurally diverse NMDA receptor subunit-specific positive allosteric modulators. Neuropharmacology, vol. 202, article 108840. https://doi.org/10.1016/j.neuropharm.2021.108840 (In English)
Frankfurt, M., Luine, V. (2015) The evolving role of dendritic spines and memory: Interaction(s) with estradiol. Hormones and Behavior, vol. 74, pp. 28–36. https://doi.org/10.1016/j.yhbeh.2015.05.004 (In English)
Gehrand, A. L., Phillips, J., Malott, K., Raff, H. (2020) Corticosterone, adrenal, and the pituitary-gonadal axis in neonatal rats: Effect of maternal separation and hypoxia. Endocrinology, vol. 161, no. 7, article bqaa085. https://doi.org/10.1210/endocr/bqaa085 (In English)
Giannopoulou, I., Pagida, M. A., Briana, D. D., Panayotacopoulou, M. T. (2018) Perinatal hypoxia as a risk factor for psychopathology later in life: The role of dopamine and neurotrophins. Hormones, vol. 17, no. 1, pp. 25–32. https://doi.org/10.1007/s42000-018-0007-7 (In English)
Goel, N., Philippe, T. J., Chang, J. et al. (2022) Cellular and serotonergic correlates of habituated neuroendocrine responses in male and female rats. Psychoneuroendocrinology, vol. 136, article 105599. https://doi.org/10.1016/j.psyneuen.2021.105599 (In English)
Kempermann, G. (2022) What is adult hippocampal neurogenesis good for? Frontiers in Neuroscience, vol. 16, article 852680. https://doi.org/10.3389/fnins.2022.852680 (In English)
Khodanovich, M., Kisel, A., Kudabaeva, M. et al. (2018) Effects of fluoxetine on hippocampal neurogenesis and neuroprotection in the model of global cerebral ischemia in rats. International Journal of Molecular Science, vol. 19, no. 1, article 162. https://doi.org/10.3390/ijms19010162 (In English)
Khozhai, L. I., Otellin, V. A. (2022) Distribution of GABAergic neurons and expression levels of GABA transporter 1 in the rat neocortex during the neonatal period after perinatal hypoxic exposure. Journal of Evolutionary Biochemistry and Physiology, vol. 58, no. 6, pp. 1687–1696. https://doi.org/10.1134/S0022093022060023 (In English)
Knox-Concepcion, K. R., Figueroa, J. D., Hartman, R. E. et al. (2019) Repression of the glucocorticoid receptor increases hypoxic-ischemic brain injury in the male neonatal rat. International Journal of Molecular Sciences, vol. 20, no. 14, article 3493. https://doi.org/10.3390/ijms20143493 (In English)
Kuhn, H. G., Toda, T., Gage, F. H. (2018) Adult hippocampal neurogenesis: A coming-of-age story. Journal of Neuroscience, vol. 38, no. 49, pp. 10401–10410. https://doi.org/10.1523/JNEUROSCI.2144-18.2018 (In English)
Lipner, E., O’Brien, K. J., Pike, M. R. et al. (2023) Environmental risk factors and cognitive outcomes in psychosis: Pre-, perinatal, and early life adversity. In: D. M. Barch, J. W. Young (eds.). Cognitive functioning in schizophrenia: Leveraging the RDoC Framework. Current topics in behavioral neurosciences. Vol. 63. Cham: Springer Publ., pp. 205–240. https://doi.org/10.1007/7854_2022_378 (In English)
Masachs, N., Charrier, V., Farrugia, F. et al. (2021) The temporal origin of dentate granule neurons dictates their role in spatial memory. Molecular Psychiatry, vol. 26, no. 12, pp. 7130–7140. https://doi.org/10.1038/s41380-021-01276-x (In English)
Millar, L. J., Shi, L., Hoerder-Suabedissen, A., Molnár, Z. (2017) Neonatal hypoxia ischemia: Mechanisms, models, and therapeutic challenges. Frontiers in Cell Neuroscience, vol. 11, article 78. https://doi.org/10.3389/fncel.2017.00078 (In English)
Morris, R. G. M. (1981) Spatial localization does not require the presence of local cues. Learning and Motivation, vol. 12, no. 2, pp. 239–260. https://doi.org/10.1016/0023-9690(81)90020-5 (In English)
Muntsant, A., Shrivastava, K., Recasens, M., Giménez-Llort, L. (2019) Severe perinatal hypoxic-ischemic brain injury induces long-term sensorimotor deficits, anxiety-like behaviors and cognitive impairment in a sex-, age-and task-selective manner in C57BL/6 mice but can be modulated by neonatal handling. Frontiers in Behavior Neuroscience, vol. 13, article 7. https://doi.org/10.3389/fnbeh.2019.00007 (In English)
Park, S. H., Lee, Y.-S., Yang, H.-J., Song, G. J. (2021) Fluoxetine potentiates phagocytosis and autophagy in microglia. Frontiers in Pharmacology, vol. 12, article 770610. https://doi.org/10.3389/fphar.2021.770610 (In English)
Philippe, T. J., Bao, L., Koblanski, M. E., Viau, V. (2022) Sex differences in serotonin 5-HT 1A receptor responses to repeated restraint stress in adult male and female rats. International Journal of Neuropsychopharmacology, vol. 25, no. 10, pp. 863–876. https://doi.org/10.1093/ijnp/pyac046 (In English)
Ramsteijn, A. S., Van de Wijer, L., Rando, J. et al. (2020) Perinatal selective serotonin reuptake inhibitor exposure and behavioral outcomes: A systematic review and meta-analyses of animal studies. Neuroscience and Biobehavioral Reviews, vol. 114, pp. 53–69. https://doi.org/10.1016/j.neubiorev.2020.04.010 (In English)
Rotem-Kohavi, N., Oberlander, T. F. (2017) Variations in neurodevelopmental outcomes in children with prenatal SSRI antidepressant exposure. Birth Defects Research, vol. 109, no. 12, pp. 909–923. https://doi.org/10.1002/bdr2.1076 (In English)
Rybnikova, E., Nalivaeva, N. (2021) Glucocorticoid-dependent mechanisms of brain tolerance to hypoxia. International Journal of Molecular Neuroscience, vol. 22, no. 15, article 7982. https://doi.org/10.3390/ijms22157982 (In English)
Sanches, E. F., Arteni, N. S., Nicola, F. et al. (2013) Early hypoxia-ischemia causes hemisphere and sex-dependent cognitive impairment and histological damage. Neuroscience, vol. 237, no. 15, pp. 208–215. https://doi.org/10.1016/j.neuroscience.2013.01.066 (In English)
Semenov, D. G., Belyakov, A. V., Rybnikova, E. A. (2022) Experimental modeling of damaging and protective hypoxia of the mammalian brain. Journal of Evolutionary Biochemistry and Physiology, vol. 58, no. 6, pp. 2021–2034. https://doi.org/10.1134/S0022093022060291 (In English)
Sukhanova, Iu. A., Sebentsova, E. A., Khukhareva, D. D. et al. (2019) Early-life N-arachidonoyl-dopamine exposure increases antioxidant capacity of the brain tissues and reduces functional deficits after neonatal hypoxia in rats. International Journal of Developmental Neuroscience, vol. 78, no. 1, pp. 7–18. https://doi.org/10.1016/j.ijdevneu.2019.06.007 (In English)
Toda, T., Gage, F. H. (2018) Review: Adult neurogenesis contributes to hippocampal plasticity. Cell and Tissue Research, vol. 373, no. 3, pp. 693–709. https://doi.org/10.1007/s00441-017-2735-4 (In English)
Vorhees, C. V., Williams, M. T. (2014) Assessing spatial learning and memory in rodents. ILAR Journal, vol. 55, no. 2, pp. 310–332. https://doi.org/10.1093/ilar/ilu013 (In English)
Yavas, E., Gonzalez, S., Fanselow, M. S. (2019) Interactions between the hippocampus, prefrontal cortex, and amygdala support complex learning and memory. F1000Research, vol. 8, article 1292. https://doi.org/10.12688/f1000research.19317.1 (In English)
Zhuravin, I. A., Dubrovskaya, N. M., Vasilev, D. S. et al. (2019) Prenatal hypoxia produces memory deficits associated with impairment of long-term synaptic plasticity in young rats. Neurobiology of Learning and Memory, vol. 164, article 107066. https://doi.org/10.1016/j.nlm.2019.107066 (In English)
Downloads
Published
Issue
Section
License
Copyright (c) 2023 Irina P. Butkevich, Viktor A. Mikhailenko, Elena A. Vershinina
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
The work is provided under the terms of the Public Offer and of Creative Commons public license Attribution-NonCommercial 4.0 International (CC BY-NC 4.0). This license allows an unlimited number of persons to reproduce and share the Licensed Material in all media and formats. Any use of the Licensed Material shall contain an identification of its Creator(s) and must be for non-commercial purposes only.
