Skip to main content
Log in

Ultrastructural Alterations in the Sensorimotor Cortex upon Delayed Development of Motor Behavior in Early Ontogenesis of Rats Exposed to Prenatal Hypoxia

  • Published:
Cell and Tissue Biology Aims and scope Submit manuscript

Abstract—

A comparative study of morphogenesis and synaptogenesis of the sensorimotor cortex and changes in motor behavior during early ontogenesis (Р5, Р14) of rats with normal development and rats subjected to prenatal hypoxia at Е14 (7% O2, 3 h) has been performed. The rats subjected to prenatal hypoxia exhibited delayed maturation of neural elements of the sensorimotor cortex in the first 2 weeks of postnatal ontogenesis. The following signs of nervous tissue immaturity were revealed in the neuropil of the sensorimotor cortex: a large volume of extracellular space, multiple growth cones, insufficient neuronal differentiation, lack of mature synapses, single spines without spine apparatus, and contacts between processes in the form of desmosomes. In addition to delayed formation of neural elements, 14-day-old rats subjected to prenatal hypoxia had signs of nerve cell destruction: hyperchromatosis, chromatolysis with organelle lysis, and destruction of the outer membrane. Prenatal hypoxia is a severe stress factor and has been shown to cause delayed development of motor activity in rat pups in early ontogenesis, such as a delayed reaction of forelimb placing on the surface and reduced total spontaneous motor activity. A comparison of the results with previous data on similar changes in the dorsolateral striatum leads to the conclusion that the action of the adverse factor during embryogenesis causes morphological and functional delay in formation of corticostriatal system elements, leading to impaired development of motor behavior and disturbance of coordinated responses in animals.

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.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Allam, A.A. and Abo-Eleneen, R.E., The development of sensorimotor reflexes in albino mice; albino rats and black-hooded rats, Int. J. Dev. Neurosci., 2012, vol. 30, pp. 545–553.

    Article  PubMed  Google Scholar 

  2. De Ryck, M., Van Reempts, J., Duytschaever, H., Van Deuren, B., and Clincke, G., Neocortical localization of tactile/proprioceptive limb placing reactions in the rat, Brain Res., 1992, vol. 573, pp. 44–60.

    Article  PubMed  CAS  Google Scholar 

  3. Dubrovskaya, N.M. and Zhuravin, I.A., Ontogenetic characteristics of behavior in rats subjected to hypoxia on day 14 or day 18 of embryogenesis, Neurosci. Behav. Physiol., 2010, vol. 40, no. 2, pp. 231−238.

  4. Dubrovskaya, N.M., Vasiliev, D.S., Tikhonravov, D.L., Tumanova, N.L., and Zuravin, I.A., Change of the level of a caspase-3 activity during the early ontogenesis leads to the impairment of memory and learning in adult rats, Zh. Vyssh. Nerv. Deyat., 2017, vol. 67, no. 6, pp. 693–704.

    Google Scholar 

  5. Fan, L.W., Chen, R.F., Mitchell, H.J., Lin, R.C., Simpson, K.L., Rhodes, P.G., and Cai, Z., Alpha-Phenyl-n-tert-butyl-nitrone attenuates lipopolysaccharide-induced brain injury and improves neurological reflexes and early sensorimotor behavioral performance in juvenile rats, J. Neurosci. Res., 2008, vol. 86, pp. 3536–3547.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Nyakas, C., Buwalda, B., and Luiten, P.G.M., Hypoxia and brain development, Prog. Neurobiol., 1996, vol. 49, pp. 1–51.

    Article  PubMed  CAS  Google Scholar 

  7. Otellin, V.A., Hojai, L.I., Gilerovich, E.G., Korjevskiy, D.E., Kostkin, V.B., and Belostotskaya, G.B., Destructive actions in critical periods of prenatal ontogenesis as a factor affecting development of brain structure and behavior after birth, Vestn. Ross. Akad. Med. Nauk, 2002, vol. 12, pp. 32–35.

    Google Scholar 

  8. Paxinos, G. and Watson, C., The Rat Brain in Stereotaxic Coordinates, Elsevier, 2007, 6th ed.

    Google Scholar 

  9. Rakic, P., Radial versus tangential migration of neuronal clones in the developing cerebral cortex, Proc. Natl. Acad. Sci. U. S. A., 1995, vol. 92, pp. 11323–11327.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Reid, C.B. and Walsh, C.A., Evidence of common progenitors and patterns of dispersion in rat striatum and cerebral cortex, J. Neurosci., 2002, vol. 22, pp. 4002–4014.

    Article  PubMed  CAS  Google Scholar 

  11. Schallert, T., Behavioral tests for preclinical intervention assessment, NeuroRX, 2006, vol. 3, pp. 497–504.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sokolova, N.A., Graf, A.V., Maslova, M.V., and Khyrazova, E.S., Stress na rannikh stadiyakh ontogeneza: peptidergicheskaya korrektsiya (Stress in Early Ontogenesis: Peptidergic Treatment), Moscow: T-vo Nauch. Izd. KMK, 2016.

  13. Vasilev, D.S., Dubrovskaya, N.M., Tumanova, N.L., and Zhuravin, I.A., Prenatal hypoxia in different periods of embryogenesis differentially affects cell migration, neuronal plasticity and rat behavior in postnatal ontogenesis, Front. Neurosci., 2016, vol. 10, p. 126.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Vasilyev, D.S., Tumanova, N.L., and Zhuravin, I.A., Structural alterations in cortical tissue in ontogenesis of rats subjected by hypoxia in different period of ontogenesis, J. Evol. Biochem. Physiol., 2008, vol. 44, no. 3, pp. 304–315.

  15. Zharskaya, V.D., Golikova, T.V., Lenkov, D.N., and Vereschak, N.I., Structural and functional correlates in postnatal development of rat frontal cortex areas, in Razvivayushchiisya mozg (Developing Brain), Moscow: Red. Inst. Mozga, 1984, vol. p 27–30.

  16. Zhuravin, I.A., Tumanova, N.L., Ozirskaya, E.V., Vasil’ev, D.S., and Dubrovskaya, N.M., Formation of the structural and ultrastructural organization of the striatum in early postnatal ontogenesis of rats in altered conditions of embryonic development, Neurosci. Behav. Physiol., 2006, vol. 36, no. 5, pp. 473–478.

  17. Zhuravin, I.A., Tumanova, N.L., Ozirskaya, E.V., Vasil’ev, D.S., and Dubrovskaya, N.M., Formation of striatum structural and ultrastructural organization in rat postnatal ontogenesis at changes of conditions of their embryonic development, J. Evol. Biochem. Physiol., 2007, vol. 43, no. 2, pp. 229—239.

Download references

ACKNOWLEDGMENTS

We thank O.S. Alekseeva for assistance in conducting hypoxic exposure on pregnant female rats and E.V. Ozirskaya for assistance in preparation of electron microscopy specimens. The electron microscopic study was performed at the Center of Joint Facilities for Physiological, Biochemical, and Molecular Biological Research of the Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences.

This study was performed within the framework of a state assignment of the Federal Agency for Scientific Organizations (АААА-А18-118012290373-7) and partially supported by the Russian Foundation for Basic Research (project no. 16-04-00694).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. S. Vasil’ev.

Additional information

Translated by M. Novikova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tumanova, N.L., Vasil’ev, D.S., Dubrovskaya, N.M. et al. Ultrastructural Alterations in the Sensorimotor Cortex upon Delayed Development of Motor Behavior in Early Ontogenesis of Rats Exposed to Prenatal Hypoxia. Cell Tiss. Biol. 12, 419–425 (2018). https://doi.org/10.1134/S1990519X18050097

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990519X18050097

Keywords:

Navigation