Skip to main content
Log in

Age- and Sex-Related Features of the Behavior of Prenatally Stressed Rats Using a Dark/Light Modification of the Behavioral “Suok” Test

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

We report here studies of exploratory activity, anxiety, and motor disintegration in prenatally stressed immature and adult male and female rats using the Suok test method. Female rats at pregnancy days 16–19 were placed for 3 h in plastic pencil cases to impose restraint on the animals. Offspring were tested at 20 and 120 days of postnatal ontogenesis. Testing of adult females took account of the estrous cycle. Anxiety decreased and exploratory activity increased in all experimental groups, with the exception of adult females in diestrus. At this stage of the estrous cycle, females showed behavioral patterns characterized by anxiety and decreased exploratory behavior. Sensorimotor disintegration, characteristic of immature animals of the experimental groups, settled with age, but not in females in diestrus. Thus, the results obtained here lead to the conclusion that prenatal stress can have both adaptive functions, increasing exploratory behavior, and maladaptive functions. Prenatal stress-induced anxiolytic effects could be negative, impairing evolutionarily significant protective mechanisms, or beneficial, depending on environmental conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bagheri, M., Saboory, E., Nejatbakhsh, M., et al., “Prenatal stress increased γ2 GABAA receptor subunit gene expression in hippocampus and potentiated pentylenetetrazol-induced seizure in rats,” Iran J. Basic Med. Sci., 23, 724–729 (2020).

    PubMed  PubMed Central  Google Scholar 

  • Bazhanova, E. D., Anisimov, V. N., Sukhanova, D. S., and Teplyi, D. L., “A comparative study of the effect of drugs that improve brain metabolism (Angiogen, Cytoflavin) on the processes of neuron apoptosis and brain function during aging and in experimental studies,” Eksperim. Klin. Farmakol., 78, No. 2, 58–64 (2015).

    Google Scholar 

  • Bredy, T. W., Grant, R. J., Champagne, D. L., and Meaney, M. J., “Maternal care influences neuronal survival in the hippocampus of the rat,” Eur. J. Neurosci., 18, No. 10, 2903–2909 (2003).

    Article  PubMed  Google Scholar 

  • Buresh, Ya., Bureshova, O., and Houston, D. P., Methods and Basic Experiments in Research on the Brain and Behavior, Vysshaya Shkola, Moscow (1991).

  • Dion, A., Munoz, P. T., and Franklin, T. B., “Epigenetic mechanisms impacted by chronic stress across the rodent lifespan,” Neurobiol. Stress, 31, No. 17, 100434 (2022).

  • Ennaceur, A., “Tests of unconditioned anxiety – Pitfalls and disappointments,” Physiol. Behav., 135, 55–71 (2014).

    Article  CAS  PubMed  Google Scholar 

  • Filatova, E. V., Egorov, Yu., Kucher, E. O., and Kulagina, K. O., “The influences of individual characteristics on the formation of ethanol preference in female and male Wistar rats,” Zh. Evolyuts. Biokhim. Fiziol., 47, No. 5, 404–410 (2011).

    CAS  Google Scholar 

  • Fine, R., Zhang, J., and Stevens, H. E., “Prenatal stress and inhibitory neuron systems: implications for neuropsychiatric disorders,” Mol. Psychiatry, 19, No. 6, 641–51 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gur, T. L., Palkar, A. V., Rajasekera, T., et al., “Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring,” Behav. Brain Res., 1, 886–894 (2019).

    Article  Google Scholar 

  • Inoue, S., “Neural basis for estrous cycle-dependent control of female behaviors,” Neurosci. Res., 176, 1–8 (2022).

    Article  PubMed  Google Scholar 

  • Kabak, Ya. M., Endocrinology Workshop, Moscow State University Press, Moscow (1968).

  • Kade, A. Kh., Kravchenko, S. V., Trofimenko, A. I., et al., “Modern methods for assessing the level of anxiety in rodents in behavioral tests based on models without prior conditioning,” Kuban. Nauchn. Vestn., 25, No. 6, 171–176 (2018).

    Article  Google Scholar 

  • Kalueff, A. V. and Tuohimaa, P., “The Suok (‘ropewalking’) murine test of anxiety,” Brain Res. Brain Res. Protoc., 14, No. 2, 87–99 (2005).

    Article  PubMed  Google Scholar 

  • Kalueff, A. V., Keisala, T., Minasyan, A., et al., “The regular and light–dark Suok tests of anxiety and sensorimotor integration: utility for behavioral characterization in laboratory rodents,” Nat. Protoc., 3, 129–136 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Kalueff, A. V., Minasyan, A., and Tuohimaa, P., “Behavioural characterization in rats using the elevated alley Suok test,” Behav. Brain Res., 165, No. 1, 52–57 (2005).

    Article  PubMed  Google Scholar 

  • Kaluev, A. V. and Tuokhimaa, P., “Suok test – a new behavioral model of anxiety,” Neironauki, 1, 17–23 (2005).

    Google Scholar 

  • Kreutzmann, J. C. and Fendt, M., “Intranasal oxytocin compensates for estrus cycle-specific reduction of conditioned safety memory in rats: Implications for psychiatric disorders,” Neurobiol. Stress, 14, 17–20 (2021).

    Article  Google Scholar 

  • Kundakovic, M. and Rocks, D., “Sex hormone fluctuation and increased female risk for depression and anxiety disorders: From clinical evidence to molecular mechanisms,” Front. Neuroendocrinol., 66, 101010 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lautarescu, A., Craig, M. C., and Glover, V., “Prenatal stress: Effects on fetal and child brain development,” Int. Rev. Neurobiol., 150, 17–40 (2020).

    Article  PubMed  Google Scholar 

  • Markel’, A. L., “Assessment of the main characteristics of the behavior of rats in the open field,” Zh. Vyssh. Nerv. Deyat., 31, No. 2, 301–307 (1981).

  • Maur, D. G., Romero, C. B., Burdet, B., et al., “Prenatal stress induces alterations in cerebellar nitric oxide that are correlated with deficits in spatial memory in rat’s offspring,” Neurochem. Int., 61, 1294–1301 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Miller, C. K., Halbing, A. A., Patisaul, H. B., and Meitzen, J., “Interactions of the estrous cycle, novelty, and light on female and male rat open field locomotor and anxiety-related behaviors,” Physiol. Behav., 228, No. 1, 113203 (2021).

  • Moura, C. A., Oliveira, M. C., and Costa, L. F., “Prenatal restraint stress impairs recognition memory in adult male and female offspring,” Acta Neuropsychiatr., 32, No. 3, 122–127 (2020).

    Article  Google Scholar 

  • Mukai, H., Takata, N., Ishii, H. T., et al., “Hippocampal synthesis of estrogens and androgens which are paracrine modulators of synaptic plasticity: synaptocrinology,” Neuroscience, 138, No. 3, 757 (2006).

    Google Scholar 

  • Ordyan, N. E., Pivina, S. G., Mironova, V. I., et al., “Hormonal and behavioral characteristics of prenatally stressed female rats in an experimental model of depression,” Ros. Fiziol. Zh., 103, No. 8, 873–883 (2017).

    Google Scholar 

  • Pallares, E. M., Bernasconi, P. A. S., Feleder, C., and Cutrera, R. A., “Effects of prenatal stress on motor performance and anxiety behavior in Swiss mice,” Physiol. Behav., 92, No. 5, 951–956 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Pavlova, I. V. and Rysakova, M. P., “Signs of anxiety in Wistar rats during the development of conditioned reflex fear,” Zh. Vyssh. Nerv. Deyat., 65, No. 6, 720–734 (2015).

    CAS  Google Scholar 

  • Pivina, S. G., Fedotova, Yu. O., Akulova, V. K., and Ordyan, N. E., “Effects of selective serotonin reuptake inhibitors on anxiety behavior and pituitary-adrenal axis activity in prenatally stressed male rats,” Neirokhimiya, 28, No. 1, 55–59 (2011).

    Google Scholar 

  • Rogovin, K. A., “Stress in early ontogenesis as an adaptive phenomenon,” Zh. Obsh. Biol., 80, No. 2, 95–123 (2019).

    Google Scholar 

  • Samotrueva, M. A., Teplyi, D. L., Tyurenkov, I. N., and Luzhnova, S. A., “Changes in the psychoemotional state in conditions of suppression of immunogenesis and correction of disorders with GABA-positive agents,” Ros. Fiziol. Zh., 96, No. 2, 115–20 (2010).

    CAS  Google Scholar 

  • Sashkov, V. A., “Relationship between brain sex steroid levels and behavior and anxiety in female rats with different hormonal status,” Vestn. Nov. Med. Tekhnol., 16, No. 3, 21–25 (2009).

    Google Scholar 

  • Shalyapina, V. G., Zaichenko, I. N., Batuev, A. C., and Ordyan, N. E., “Changes in the neuroendocrine regulation of adaptive behavior after stress in late prenatal ontogenesis,” Ros. Fiziol. Zh., 87, No. 9, 1193–1201 (2001).

    CAS  Google Scholar 

  • Soares-Cunha, C., Coimbra, B., Borges, S., et al., “Mild prenatal stress causes emotional and brain structural modifications in rats of both sexes,” Front. Behav. Neurosci., 12, 129 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • Sokolova, Yu. O., Teplyi, D. L., Anisimov, V. N., and Bazhanova, E. D., “The effects of Cytoflavin on locomotor and psychoemotional status in physiological and pathological aging,” Usp. Gerontol., 33, No. 2, 367–372 (2020).

    CAS  Google Scholar 

  • Stevens, H. E., Su, T., Yanagawa, Y., and Vaccarino, F. M., “Prenatal stress delays inhibitory neuron progenitor migration in the developing neocortex,” Psychoneuroendocrinology, 38, No. 4, 509–521 (2013).

    Article  CAS  PubMed  Google Scholar 

  • Sze, Y. and Brunton, P. J., “Effects of prenatal stress on neuroactive steroid responses to acute stress in adult male and female rats,” J. Neuroendocrinol., 33, No. 1, 12916 (2021).

  • Szuran, T., Zimmerman, E., Pliska, V., et al., “Prenatal stress effects on exploratory activity and stress-induced analgesia in rats,” Dev. Psychobiol., 24, No. 5, 361–372 (1991).

    Article  CAS  PubMed  Google Scholar 

  • Vinogradova, E. P., Arutyunyan, N. A., and Zhukov, D. A., “Anxiety and plasma progesterone at different stages of the estrous cycle in rats with opposite behavioral strategies,” Ros. Fiziol. Zh., 104, No. 5, 565–572 (2018).

    Google Scholar 

  • V’yushina, A. V. and Ordyan, N. E., “Some aspects of the current state of the problem of prenatal stress and the role of oxidative stress in mediating its consequences,” Usp. Sovr. Biol., 141, No. 2, 133–148 (2021).

  • Wu, J., Song, T.-B., Li, Y.-J., et al., “Prenatal restraint stress impairs learning and memory and hippocampal PKCbeta1 expression and translocation in offspring rats,” Brain Res., 13, 205–213 (2007).

    Article  Google Scholar 

  • Zhang, X., Tong, G., Guanghao, Y., et al., “Stress-induced functional alterations in amygdala: Implications for neuropsychiatric diseases,” Front. Neurosci., 12, 367 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. N. Kuleshova.

Additional information

Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 73, No. 4, pp. 550–562, July–August, 2023.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kuleshova, O.N. Age- and Sex-Related Features of the Behavior of Prenatally Stressed Rats Using a Dark/Light Modification of the Behavioral “Suok” Test. Neurosci Behav Physi 53, 1602–1610 (2023). https://doi.org/10.1007/s11055-023-01555-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-023-01555-w

Keywords

Navigation