Abstract
The aim of the present work was to identify the characteristics of the physiological development of the brain and the formation of behavior in rats subjected to hypoxia on day 13.5 of embryogenesis. These animals showed delayed development and changes in nerve tissue structure in the sensorimotor cortex, along with disturbances to the processes forming normal movement responses during the first month after birth. These changes were partially compensated with age, though adult animals subjected to acute prenatal hypoxia were less able to learn new complex manipulatory movements. Alterations in nerve tissue structure and changes in the neuronal composition of the sensorimotor cortex correlated with the times of appearance of behavioral impairments at different stages of ontogenesis. Thus, changes in the conditions in which the body is formed during a defined period of embryogenesis lead to abnormalities in the process of ontogenetic development and the ability to learn new movements.
Similar content being viewed by others
REFERENCES
Ya. Buresh, O. Bureshova, and J. P. Houston, Methods and Basic Experiments in Studies of the Brain and Behavior [in Russian], Moscow (1991).
N. M. Dubrovskaya and I. A. Zhuravin, “The role of the cholinergic system of the dorsal and ventral striatum of the rat brain in the regulation of learning behavior,” Ros. Fiziol. Zh. im. I. M. Sechenova, 83, No. 1-2, 83–89 (1997).
N. M. Dubrovskaya, D. O. Potapov, and N. L. Tumanova, “Effects of prenatal hypoxia on the development of rats during postnatal ontogenesis,” Vestn. Molodykh Uchenykh. 4. Seriya Nauki o Zhizni (Young Scientists News. 4. Life Sciences Series) 1, 9–15 (2002).
P. N. Ermokhin, Histopathology of the Central Nervous System. An Atlas of Microphotographs [in Russian], Meditsina, Moscow (1969).
Yu. M. Zhabotinskii, Normal and Pathological Neuron Morphology [in Russian], Meditsina, Moscow (1965).
I. A. Zhuravin, “Effects of conditions of prenatal development on the formation of the central mechanisms of regulation of motor functions,” in: Questions of Human Ecology [in Russian], Arkhangel'sk (2000), pp. 83–87.
I. A. Zhuravin, “Formation of the central mechanisms of regulation of motor functions in mammals depending on the conditions of embryonic development,” Zh. Évolyuts. Biokhim. Fiziol., 38, No. 5, 478–484 (2002).
I. A. Zhuravin and N. M. Dubrovskaya, “Involvement of the cholinergic system of the sensorimotor cortex of the rat brain in controlling different types of movement,” Zh. Vyssh. Nerv. Deyat., 50, No. 1, 103–112 (1999).
I. A. Zhuravin, N. L. Tumanova, and D. O. Potapov, “Structural changes in the sensorimotor cortex of neonatal rats after prenatal hypoxia,” Zh. Évolyuts. Biokhim. Fiziol., 37, No. 6, 518–520 (2001).
M. E. Ioffe, Corticospinal Mechanisms of Operant Motor Reactions [in Russian], Nauka, Moscow (1975).
M. E. Ioffe, Mechanisms of Motor Learning [in Russian], Nauka, Moscow (1991).
V. G. Kassil', V. A. Otellin, L. I. Khozhai, and V. B. Kostkin, “Critical periods of brain development,” Ros. Fiziol. Zh. im. I. M. Sechenova, 86, No. 11, 1418–1425 (2000).
S. M. Lavrenova, N. N. Nalivaeva, and I. A. Zhuravin, “Acetylcholinesterase activity in the sensorimotor cortex in early ontogenesis in rats subjected to prenatal hypoxia,” Zh. Évolyuts. Biokhim. Fiziol., 39, No. 2, 154–159 (2003).
E. V. Maksimova, Ontogenesis of the Cerebral Cortex [in Russian], Nauka, Moscow (1990).
N. N. Nalivaeva, B. I. Klement'ev, S. A. Plesneva, U. B. Chekulaeva, and I. A. Zhuravin,, “Effects of hypoxia on the state of cell membranes in the right and left hemispheres in rat embryos,” Zh. Évolyuts. Biokhim. Fiziol., 34, No. 4, 485–491 (1998).
S. N. Olenev, The Developing Brain. Cellular, Molecular, and Genetic Aspects of Neuroembryology [in Russian], Nauka, Leningrad (1978).
G. M. Savel'eva, L. G. Sichinava, G. D. Dzhivilegova, and G. I. Shalina, “Perinatal hypoxic lesions of the CNS in neonates,” Vestn. Ros. Akad. Med. Nauk, 1, 20–23 (1994).
M. O. Samoilov, Responses of Brain Neurons to Hypoxia [in Russian], Nauka, Leningrad (1985).
P. G. Svetlov, “The theory of critical periods of development and its value for understanding the principles of action of the environment on ontogenesis,” in: Questions in Cytology and General Physiology [in Russian], Academy of Sciences of the USSR Press, Moscow, Leningrad (1960).
J. Altman and K. Sudarshan, “Postnatal development of locomotion in the laboratory rat,” Anim. Behav., 23, 896–920 (1975).
R. G. Boutilier and J. St.-Pierre, “Surviving hypoxia without really dying,” Comp. Biochem. Physiol. A. Molecular and Integrative Physiology, 126, No. 4, 481–490 (2000).
J. B. Brierley, “Cerebral hypoxia,” in: Greenfield's Neuropathology, W. Blackwood and A. Corsellis (eds.), Arnold, London (1976), pp. 43–85.
R. E. Burke and K. G. Bainbridge, “Relative loss of the striatal striosome compartment, defined by calbindin-D28k immunostaining, following developmental hypoxic-ischemic injury,” Neurosci., 56, No. 2, 305–315 (1993).
D. W. Choi, “Cerebral hypoxia: some new approaches and unanswered questions,” J. Neurosci., 10, 2493–2501 (1990).
J. M. Donatelle, “Growth of the corticospinal tract and development of placing reactions in the postnatal rat,” J. Comp. Neurol., 175, No. 2, 207–232 (1977).
D. Grisaru, M. Sternfeld, A. Eldor, D. Glick, and H. Soreq, “Structural roles of acetylcholinesterase variants in biology and pathology,” Eur. J. Biochem., 264, 672–686 (1999).
J. M. Gleadle and P. J. Ratcliffe, “Hypoxia and the regulation of gene expression,” Mol. Med. Today, 4, No. 3, 122–129 (1998).
E. M. Jansen and W. C. Low, “Quantitative analysis of contralateral hemisphere hypertrophy and sensorimotor performance in adult rat following unilateral neonatal ischemic-hypoxic brain injury,” Brain Res., 708, 399–403 (1996).
E. A. Joosten, A. A. Gribnau, and P. J. Dederen, “An anterograde tracer study of the developing corticospinal tract in the rat: three components,” Dev. Brain Res., 36, 121–132 (1987).
P. Lipton, “Ischemic cell death in brain neurons,” Physiol. Rev., 79, 1431–1568 (1999).
L. J. Martin, A. Brambrink, R. C. Koehler, and J. Traystman, “Primary sensory and forebrain motor systems in the newborn brain are preferentially damaged by hypoxia-ischemia,” J. Comp. Neurol., 377, No. 2, 262–285 (1997).
O. P. Mishra and M. Delivoria-Papadopoulos, “Cellular mechanisms of hypoxic injury in the developing brain,” Brain Res. Bull., 48, 233–238 (1999).
D. Mu, W. Liang, G. Zhang, and X. Wu, “The relationship between the c-jun mRNA expression and apoptosis of neurons in rat brain following perinatal ischemic-hypoxia,” Chin. Med. J. (Engl.), 112, No. 1, 40–43 (1999).
C. Nyakas, B. Buwalda, and P. D. M. Luiten, “Hypoxia and brain development,” Prog. Neurobiol., 49, No. 1, 1–51 (1996).
C. A. Piantadosi, J. Zhang, E. D. Levin, R. J. Folz, and D. E. Schmechel, “Apoptosis and delayed neuronal damage after carbon monoxide poisoning in the rat,” Exptl. Neurol., 147, No. 1, 103–114 (1997).
J. Saez-Valero, G. Sberna, C. A. Mclean, and D. H. Small, “Molecular isoform distribution and glycosylation of acetylcholinesterase are altered in brain and cerebrospinal fluid of patients with Alzheimer's disease,” J. Neurochem., 72, 1600–1608 (1999).
M. Schwab, R. Schaller, R. Bauer, and U. Zwiener, “Morphofunctional effects of moderate forebrain ischemia combined with short-term hypoxia in rats-protective effects of Cerebrolysin,” Exptl. Toxicol. Pathol., 49, No. 1-2, 29–37 (1997).
K. V. Sharma, C. Koenigsberger, S. Brimijoin, and J. W. Bigbee, “Direct evidence for an adhesive function in the noncholinergic role of acetylcholinesterase in neurite outgrowth,” J. Neurosci. Res., 63, 165–175 (2001).
H. Soreq and S. Seidman, “Acetylcholinesterase-new roles for an old actor,” Nature Rev. Neurosci., 2, 294–302 (2001).
F. Thullier, R. Lalonde, X. Cousin, and F. Lestienne, “Neurobehavioral evaluation of lurcher mutant mice during ontogeny,” Dev. Brain Res., 100, 22–28 (1997).
D. Trotti, N. C. Danbolt, and A. Volterra, “Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration?” Trends Pharmacol. Sci., 19, 328–334 (1998).
S. P. Wise and P. J. Donoghue, “Motor cortex of rodent,” in: Sensory-Motor Areas and Aspects of Cortical Connectivity, E. G. Jones, and A. Pteres (eds.), Plenum Press, London (1986), pp. 243–270.
I. A. Zhuravin, N. M. Dubrovskaya, and S. A. Plesneva, “Striatal level of regulation of learned forepaw movements in rats,” Physiol. Res., 51, Suppl. 1, S67–S76 (2002).
Rights and permissions
About this article
Cite this article
Zhuravin, I.A., Dubrovskaya, N.M. & Tumanova, N.L. Postnatal Physiological Development of Rats after Acute Prenatal Hypoxia. Neurosci Behav Physiol 34, 809–816 (2004). https://doi.org/10.1023/B:NEAB.0000038132.08219.31
Issue Date:
DOI: https://doi.org/10.1023/B:NEAB.0000038132.08219.31