UDC

57.012.4

DOI

10.37482/2687-1491-Z034

Authors

Svetlana Yu. Filippova* ORCID: 0000-0002-4558-5896
Aleksandr K. Logvinov* ORCID: 0000-0002-8873-3625
Evgeniya Yu. Kirichenko* ORCID: 0000-0003-4703-1616
*Academy of Biology and Biotechnologies named after D.I. Ivanovsky, Southern Federal University (Rostov-on-Don, Russian Federation)
Corresponding author: Svetlana Filippova, address: prosp. Stachki 194/1, Rostov-on-Don, 344090, Russian Federation; e-mail: filsv@yandex.ru

Abstract

Astrocytes are the main glial cells maintaining water-electrolyte and energy balance in the brain. Today, astroglia is also believed to take a direct part in the regulation of synaptic transmission and in enabling synchronous operation of neurons at large distances. Astrocytes fulfil their functions through numerous processes that penetrate the entire neuropil. The authors believe that changes in the astrocyte membrane surface area per unit volume of neuropil directly reflect changes in the intensity of the astrocyte–neuron interaction. Strengthening or weakening of astrocyte regulation, undoubtedly, affect the functioning of neural circuits. Nevertheless, in spite of the growing popularity of research into the glia–neuron relations, this aspect remains insufficiently studied when it comes to the cerebral cortex. The purpose of this study was to layer-by-layer determine the astrocyte membrane surface per unit volume in the neuropil of the rat primary somatosensory cortex. The research was conducted on samples of the primary somatosensory cortex obtained from 5 white male rats (P60–80). After immune labelling against astrocytic marker S100B using the pre-embedding method, the samples were prepared for transmission electron microscopy according to the standard technique. In total, 250 electron micrographs were obtained for each layer of the primary somatosensory cortex, which were then used to determine the astrocyte membrane surface area per unit volume in the neuropil by means of the random secant method. The research found that this indicator is the minimum in the first and maximum in the fifth layers of the cortical column. In addition, the article discusses the possible functional consequences of uneven distribution of astrocytic membranes in the neocortex.

Keywords

primary somatosensory cortex, astrocyte, cortical column, transmission electron microscopy

References

1. Gomazkov O.A. Astrotsity kak posredniki integratsionnykh protsessov v mozge [Astrocytes as Mediators of Integration Processes in the Brain]. Uspekhi sovremennoy biologii, 2018, vol. 138, no. 4, pp. 373–382. DOI: 10.7868/S004213241804004X
2. Araque A., Parpura V., Sanzgiri R.P., Haydon P.G. Tripartite Synapses: Glia, the Unacknowledged Partner. Trends Neurosci., 1999, vol. 22, no. 5, pp. 208–215.
3. Kushnireva L.A., Korkotyan E.A., Sem’yanov A.V. Nezasluzhenno zabytye: mesto glial’nykh kletok v gipotezakh vozniknoveniya bolezni Al’tsgeymera [Undeservedly Forgotten: the Place of Glial Cells Among the Hypothesеs of Alzheimer’s Disease]. Rossiyskiy fiziologicheskiy zhurnal im. I.M. Sechenova, 2019, vol. 105, no. 9, pp. 1067–1095. DOI: 10.1134/S0869813919090085
4. Kolomeets N.S., Uranova N.A. Sovremennye predstavleniya o reaktivnosti astrotsitov pri shizofrenii [Current Conceptions About Astrocyte Reactivity in Schizophrenia]. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova, 2014, no. 5, pp. 92–99.
5. Blanco-Suárez E., Caldwell A.L.M., Allen N.J. Role of Astrocyte-Synapse Interactions in CNS Disorders. J. Physiol., 2017, vol. 595, no. 6, pp. 1903–1916.
6. Steinhäuser C., Seifert G., Bedner P. Astrocyte Dysfunction in Temporal Lobe Epilepsy: K+ Channels and Gap Junction Coupling. Glia, 2012, vol. 60, no. 8, pp. 1192–1202.
7. Tong X., Ao Y., Faas G.C., Nwaobi S.E., Xu J., Haustein M.D., Anderson M.A., Mody I., Olsen M.L., Sofroniew M.V., Khakh B.S. Astrocyte Kir4.1 Ion Channel Deficits Contribute to Neuronal Dysfunction in
Huntington’s Disease Model Mice. Nat. Neurosci., 2014, vol. 17, no. 5, pp. 694–703.
8. Coulter D.A., Eid T. Astrocytic Regulation of Glutamate Homeostasis in Epilepsy. Glia, 2012, vol. 60, no. 8, pp. 1215–1226.
9. Scofield M.D., Kalivas P.W. Astrocytic Dysfunction and Addiction: Consequences of Impaired Glutamate Homeostasis. Neuroscientist, 2014, vol. 20, no. 6, pp. 610–622.
10. Harada K., Kamiya T., Tsuboi T. Gliotransmitter Release from Astrocytes: Functional, Developmental, and Pathological Implications in the Brain. Front. Neurosci., 2016, vol. 9. Art. no. 499.
11. Allen N.J. Astrocyte Regulation of Synaptic Behavior. Annu. Rev. Cell Dev. Biol., 2014, vol. 30, pp. 439–463.
12. Bélanger S., de Souza B.O., Casanova C., Lesage F. Correlation of Hemodynamic and Fluorescence Signals Under Resting State Conditions in Mice’s Barrel Field Cortex. Neurosci. Lett., 2016, vol. 616, pp. 177–181.
13. Stobart J.L., Ferrari K.D., Barrett M.J.P., Glück C., Stobart M.J., Zuend M., Weber B. Cortical Circuit Activity Evokes Rapid Astrocyte Calcium Signals on a Similar Timescale to Neurons. Neuron, 2018, vol. 98, no. 4, pp. 726–735.
14. Morgun A.V., Malinovskaya N.A., Komleva Yu.K., Lopatina O.L., Kuvacheva N.V., Panina Yu.A., Taranushenko T.Y., Solonchuk Yu.R., Salmina A.B. Structural and Functional Heterogeneity of Astrocytes in the Brain: Role in Neurodegeneration and Neuroinflammation. Bull. Sib. Med., 2014, vol. 13, no. 5, pp. 138–148 (in Russ.).
15. John Lin C.C., Yu K., Hatcher A., Huang T.W., Lee H.K., Carlson J., Weston M.C., Chen F., Zhang Y., Zhu W., Mohila C.A., Ahmed N., Patel A.J., Arenkiel B.R., Noebels J.L., Creighton C.J., Deneen B. Identification of Diverse Astrocyte Populations and Their Malignant Analogs. Nat. Neurosci., 2017, vol. 20, no. 3, pp. 396–405.
16. Pestana F., Edwards-Faret G., Belgard T.G., Martirosyan A., Holt M.G. No Longer Underappreciated: The Emerging Concept of Astrocyte Heterogeneity in Neuroscience. Brain Sci., 2020, vol. 10, no. 3. Art. no. 168.
17. Lanjakornsiripan D., Pior B.J., Kawaguchi D., Furutachi S., Tahara T., Katsuyama Y., Suzuki Y., Fukazawa Y., Gotoh Y. Layer-Specific Morphological and Molecular Differences in Neocortical Astrocytes and Their Dependence on Neuronal Layers. Nat. Commun., 2018, vol. 9. Art. no. 1623.
18. Avtandilov G.G. Meditsinskaya morfometriya [Medical Morphometry]. Moscow, 1990. 384 p.
19. López-Hidalgo M., Schummers J. Cortical Maps: A Role for Astrocytes? Curr. Opin. Neurobiol., 2014, vol. 24, no. 1, pp. 176–189.
20. Eilam R., Aharoni R., Arnon R., Malach R. Astrocyte Morphology Is Confined by Cortical Functional Boundaries in Mammals Ranging from Mice to Human. eLife, 2016, no. 5. Art. no. e15915.
21. Fellin T., Halassa M.M., Terunuma M., Succol F., Takano H., Frank M., Moss S.J., Haydon P.G. Endogenous Nonneuronal Modulators of Synaptic Transmission Control Cortical Slow Oscillations in vivo. Proc. Natl. Acad. Sci. USA, 2009, vol. 106, no. 35, pp. 15037–15042.
22. Foley J., Blutstein T., Lee S., Erneux C., Halassa M.M., Haydon P. Astrocytic IP3/Ca2+ Signaling Modulates Theta Rhythm and REM Sleep. Front. Neural. Circuits, 2017, vol. 11. Art. no. 3.
23. Lee H.S., Ghetti A., Pinto-Duarte A., Wang X., Dziewczapolski G., Galimi F., Huitron-Resendiz S., Piña-Crespo J.C., Roberts A.J., Verma I.M., Sejnowski T.J., Heinemann S.F. Astrocytes Contribute to Gamma Oscillations and Recognition Memory. Proc. Natl. Acad. Sci. USA, 2014, vol. 111, no. 32, pp. E3343–E3352.
24. Miyamoto D., Hirai D., Murayama M. The Roles of Cortical Slow Waves in Synaptic Plasticity and Memory Consolidation. Front. Neural Circuits, 2017, vol. 11. Art. no. 92.
25. Bosman C.A., Lansink C.S., Pennartz C.M.A. Functions of Gamma-Band Synchronization in Cognition: From Single Circuits to Functional Diversity Across Cortical and Subcortical Systems. Eur. J. Neurosci., 2014, vol. 39, no. 11, pp. 1982–1999.
26. Beltramo R., D’Urso G., Dal Maschio M., Farisello P., Bovetti S., Clovis Y., Lassi G., Tucci V., De Pietri Tonelli D., Fellin T. Layer-Specific Excitatory Circuits Differentially Control Recurrent Network Dynamics in the Neocortex. Nat. Neurosci., 2013, vol. 16, no. 2, pp. 227–234.
27. Witcher M.R., Park Y.D., Lee M.R., Sharma S., Harris K.M., Kirov S.A. Three-Dimensional Relationships Between Perisynaptic Astroglia and Human Hippocampal Synapses. Glia, 2010, vol. 58, no. 5, pp. 572–587.
28. Xu-Friedman M.A., Harris K.M., Regehr W.G. Three-Dimensional Comparison of Ultrastructural Characteristics at Depressing and Facilitating Synapses onto Cerebellar Purkinje Cells. J. Neurosci., 2001, vol. 21, no. 17, pp. 6666–6672.
29. Chounlamountry K., Kessler J.P. The Ultrastructure of Perisynaptic Glia in the Nucleus Tractus Solitarii of the Adult Rat: Comparison Between Single Synapses and Multisynaptic Arrangements. Glia, 2011, vol. 59, no. 4, pp. 655–663.
30. Benedetti B., Matyash V., Kettenmann H. Astrocytes Control GABAergic Inhibition of Neurons in the Mouse Barrel Cortex. J. Physiol., 2011, vol. 589, pt. 5, pp. 1159–1172.