Physiological continuum of plasticity and pathology of the nervous system

Authors

  • Natalia V. Gulyaeva Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences; Research and Clinical Center for Neuropsychiatry of Moscow Healthcare Department https://orcid.org/0000-0002-5380-7954

DOI:

https://doi.org/10.33910/2687-1270-2020-1-4-294-302

Keywords:

integrative physiology, brain, neuroplasticity, hippocampus, molecular mechanisms, pathology

Abstract

The paper explores the concept of neuroplasticity and neuropathology continuum from the perspective of integrative physiology. The commonality and pleiotropicity of the mechanisms at molecular, synaptic, cellular, and network levels is associated with high adaptive plasticity of brain regions involved in its integrative function, including learning and memory (e.g., the hippocampus). However, the price of high plasticity is the selective vulnerability of these structures to pathology. Depending on the pathology, neuroplasticity can decrease (as a result of neuronal death and neurogenesis decline, e.g. in neurodegenerative diseases) or increase (aberrant plasticity during epileptogenesis). Along with its fundamental significance for understanding processes in normal and pathological brain, the concept of neuroplasticity continuum is practically important since it allows to assess the rationale for interfering in a specific process involved in brain disease pathogenesis as well as its normal, adaptive plasticity.

References

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McEachern, J. C., Shaw, C. A. (1999) The plasticity-pathology continuum: Defining a role for the LTP phenomenon. Journal of Neuroscience Research, vol. 58, no. 1, pp. 42–61.

McEwen, B. S. (1998) Stress, adaptation, and disease: Allostasis and allostatic load. Annals of New York Academy of Sciences, vol. 840, no. 1, pp. 33–44. DOI: 10.1111/j.1749-6632.1998.tb09546.x

McEwen, B. S., Stellar, E. (1993) Stress and the individual. Mechanisms leading to disease. Archives of Internal Medicine, vol. 153, no. 18, pp. 2093–2101.

Meerson, F. Z., Pshennikova, M. G., Malyshev, I. Yu. (1996) Adaptive defense of the organism. Architecture of the structural trace and cross protective effects of adaptation. Annals of New York Academy of Sciences, vol. 793, no. 1, pp. 371–385. DOI: 10.1111/j.1749-6632.1996.tb33529.x

Piskunov, A., Stepanichev, M., Tishkina, A. et al. (2016) Chronic combined stress induces selective and long-lasting inflammatory response evoked by changes in corticosterone accumulation and signaling in rat hippocampus. Metabolic Brain Disease, vol. 31, no. 2, pp. 445–454. DOI: 10.1007/s11011-015-9785-7

Schwartzkroin, P. A. (2001) Mechanisms of brain plasticity: From normal brain function to pathology. International Review of Neurobiology, vol. 45, no. 1, pp. 1–15. DOI: 10.1016/s0074-7742(01)45004-5

Stepanichev, M. Yu., Kudryashova, I. V., Yakovlev, A. A. et al. (2005) Central administration of a caspase inhibitor impairs shuttle-box performance in rats. Neuroscience, vol. 136, no. 2, pp. 579–591. DOI: 10.1016/j.neuroscience.2005.08.010

Yakovlev, A. A., Gulyaeva, N. V. (2011) Pleiotropic functions of brain proteinases: Methodological considerations and search for caspase substrates. Biochemistry (Moscow), vol. 76, no. 10, article 1079. DOI: 10.1134/S0006297911100014

REFERENCES

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Cohen, E. J., Quarta, E., Bravi, R. et al. (2017) Neural plasticity and network remodeling: From concepts to pathology. Neuroscience, vol. 344, pp. 326–345. DOI: 10.1016/j.neuroscience.2016.12.048 (In English)

Dingledine, R., Varvel, N. H., Dudek, F. E. (2014) When and how do seizures kill neurons, and is cell death relevant to epileptogenesis? In: H. Scharfman, P. Buckmaster (eds.). Issues in clinical epileptology: A view from the bench. Dordrecht: Springer, pp. 109–122. (Advances in experimental medicine and biology. Vol. 813). DOI: 10.1007/978-94-017-8914-1_9 (In English)

Gulyaeva, N. V. (2003) Non-apoptotic functions of caspase-3 in nervous tissue. Biochemistry (Moscow), vol. 68, no. 11, pp. 1171–1180. DOI: 10.1023/b:biry.0000009130.62944.35 (In English)

Gulyaeva, N. V. (2015) Ventral hippocampus, stress and psychopathology: Translational implications. Neurochemical Journal, vol. 9, no. 2, pp. 85–94. DOI: 10.1134/S1819712415020075 (In English)

Gulyaeva, N. V. (2015 Neiroplastichnost’ i epilepsiya: sovremennye kontseptsii i mekhanismy komorbidnosti epilepsii i depressii [Neuronal plasticity and epilepsy: Modern concepts and mechanisms of epilepsy and depression comorbidity]. Zhurnal nevrologii i psikhiatrii imeni S. S. Korsakova — S. S. Korsakov Journal of Neurology and Psychiatry, vol. 115, no. 12, pp. 148–153. DOI: 10.17116/jnevro2015115112148-153 (In Russian)

Gulyaeva, N. V. (2016) Plastichnost’ mozga i konnektopatii: mekhanizmy komorbidnosti nevrologicheskikh zabolevanij i depressii [Cerebral plasticity and connectopathies: Mechanisms of comorbidity of neurological diseases and depression]. Zhurnal nevrologii i psikhiatrii imeni S. S. Korsakova — S. S. Korsakov Journal of Neurology and Psychiatry, vol. 116, no. 11, pp. 157–162. DOI: 10.17116/jnevro2016116111157-162 (In Russian)

Gulyaeva, N. V. (2017) Molecular mechanisms of neuroplasticity: An expanding universe. Biochemistry (Moscow), vol. 82, no. 3, pp. 237–242. DOI: 10.1134/S0006297917030014 (In English)

Gulyaeva, N. V. (2017) Stadijnost’ izmenenij neiroplastichnosti pri epileptogeneze na primere visochnoj epilepsii [Staging of neuroplasticity alterations during epileptogenesis (temporal lobe epileply as an example)]. Zhurnal nevrologii i psikhiatrii imeni S. S. Korsakova — S. S. Korsakov Journal of Neurology and Psychiatry, vol. 117, no. 9, pp. 10–16. DOI: 10.17116/jnevro20171179210-16 (In Russian)

Gulyaeva, N. V. (2019a) Biochemical mechanisms and translational relevance of hippocampal vulnerability to distant focal brain injury: The price of stress response. Biochemistry (Moscow), vol. 84, no. 11, pp. 1306–1328. DOI: 10.1134/S0006297919110087 (In English)

Gulyaeva, N. V. (2019b) Functional neurochemistry of the ventral and dorsal hippocampus: Stress, depression, dementia and remote hippocampal damage. Neurochemical Research, vol. 44, no. 6, pp. 1306–1322. DOI: 10.1007/s11064-018-2662-0 (In English)

Jaworski, T., Banach-Kasper, E., Gralec, K. (2019) GSK-3β at the intersection of neuronal plasticity and neurodegeneration. Neural Plasticity, vol. 2019, article 4209475. DOI: 10.1155/2019/4209475 (In English)

Kudryashov, I. E., Yakovlev, A. A., Kudryashova, I. V., Gulyaeva, N. V. (2004) Inhibition of caspase-3 blocks long-term potentiation in hippocampal slices. Neuroscience and Behavioral Physiology, vol. 34, no. 9, pp. 877–880. DOI: 10.1023/b:neab.0000042571.86110.28 (In English)

Kudryashova, I. V., Stepanichev, M. Yu., Gulyaeva, N. V. (2009) Natural activation of caspase-3 is required for the development of operant behavior in postnatal ontogenesis. Neuroscience and Behavioral Physiology, vol. 39, no. 1, pp. 65–72. DOI: 10.1007/s11055-008-9097-z (In English)

Mattson, M. P. (1998) Free radicals, calcium, and the synaptic plasticity-cell death continuum: Emerging roles of the transcription factor NFkB. International Review of Neurobiology, vol. 42, pp. 103–168. DOI: 10.1016/s0074-7742(08)60609-1 (In English)

Mattson, M. P., Duan, W. (1999) “Apoptotic” biochemical cascades in synaptic compartments: Roles in adaptive plasticity and neurodegenerative disorders. Journal of Neuroscience Research, vol. 58, no. 1, pp. 152–166. DOI: 10.1002/(SICI)1097-4547(19991001)58:1<152::AID-JNR15>3.0.CO;2-V (In English)

McEachern, J. C., Shaw, C. A. (1996) An alternative to the LTP orthodoxy: A plasticity-pathology continuum model. Brain Research Reviews, vol. 22, no. 1, pp. 51–92. DOI: 10.1016/0165-0173(96)00006-9 (In English)

McEachern, J. C., Shaw, C. A. (1999) The plasticity-pathology continuum: Defining a role for the LTP phenomenon. Journal of Neuroscience Research, vol. 58, no. 1, pp. 42–61. (In English)

McEwen, B. S. (1998) Stress, adaptation, and disease: Allostasis and allostatic load. Annals of New York Academy of Sciences, vol. 840, no. 1, pp. 33–44. DOI: 10.1111/j.1749-6632.1998.tb09546.x (In English)

McEwen, B. S., Stellar, E. (1993) Stress and the individual. Mechanisms leading to disease. Archives of Internal Medicine, vol. 153, no. 18, pp. 2093–2101. (In English)

Meerson, F. Z. (1973) Obshchii mekhanism adaptatsii i profilaktiki [The general mechanism of adaptation and prophylaxis]. Moscow: Nauka Publ., 360 p. (In Russian)

Meerson, F. Z. (1981) Adaptatsiya, stress i profilaktika [Adaptation, stress, and prophylaxis]. Moscow: Nauka Publ., 278 p. (In Russian)

Meerson, F. Z. (1986) O “tsene” adaptatsii [The “cost” of adaptation]. Patologicheskaya fiziologiya i eksperimental’naya terapiya — Pathological Physiology and Experimental Therapy, no. 3, pp. 9–19. (In Russian)

Meerson, F. Z., Pshennikova, M. G., Malyshev, I. Yu. (1996) Adaptive defense of the organism. Architecture of the structural trace and cross protective effects of adaptation. Annals of New York Academy of Sciences, vol. 793, no. 1, pp. 371–385. DOI: 10.1111/j.1749-6632.1996.tb33529.x (In English)

Piskunov, A., Stepanichev, M., Tishkina, A. et al. (2016) Chronic combined stress induces selective and long-lasting inflammatory response evoked by changes in corticosterone accumulation and signaling in rat hippocampus. Metabolic Brain Disease, vol. 31, no. 2, pp. 445–454. DOI: 10.1007/s11011-015-9785-7 (In English)

Schwartzkroin, P. A. (2001) Mechanisms of brain plasticity: From normal brain function to pathology. International Review of Neurobiology, vol. 45, no. 1, pp. 1–15. DOI: 10.1016/s0074-7742(01)45004-5 (In English)

Stepanichev, M. Yu., Kudryashova, I. V., Yakovlev, A. A. et al. (2005) Central administration of a caspase inhibitor impairs shuttle-box performance in rats. Neuroscience, vol. 136, no. 2, pp. 579–591. DOI: 10.1016/j.neuroscience.2005.08.010 (In English)

Yakovlev, A. A., Gulyaeva, N. V. (2011) Pleiotropic functions of brain proteinases: Methodological considerations and search for caspase substrates. Biochemistry (Moscow), vol. 76, no. 10, article 1079. DOI: 10.1134/S0006297911100014 (In English)

Published

2020-12-28

Issue

Section

Reviews