Laboratory of Cellular Neurobiology of Learning
Brief history and main directions of scientific work of the laboratory
The laboratory was established in 1989 on the basis of a group that conducted research on invertebrate animals, which was part of the laboratory of academician P.V. Simonov. The main directions of scientific work are cellular mechanisms of behavior organization and behavior modifications as a result of learning, cellular and molecular mechanisms of memory. Along with traditional electrophysiological methods, optical methods of recording and confocal microscopy are actively used in the laboratory. As an object of study, animals with a simple nervous system or brain slices of vertebrates are used. International cooperation with Yale University (USA) in the field of optical methods, with the University of Arizona (USA) in the analysis of neural networks of pantopus mollusks, with the Institute of Neurophysiology of the University of Bochum (Germany) and with the University of Connecticut (USA) in the field of synaptic plasticity mechanisms.
Books in English
- Balaban P.M. (2002) Declarative and procedural memory in animals with simple nervous systems. In: "Psychology at the turn of the millennium, Vol. 1: Cognitive, biological, and health perspectives" (Eds: Lars Bäckman & Claes von Hofsten). Psychology Press, pp. 1-28.
- Balaban P.M. Applicability of the reinforcement concept to studies in simple nervous systems. In: Complex Brain Functions. Conceptual Advances in Russian Neuroscience. Eds. A.M.Ivanitsky, P.M.Balaban, Harwood Academic Publishers, 2000, p.201-211.
Список сотрудников
Publication list
Papers
- Borodinova A.A., Kuznetsova M.A., Alekseeva V.S., Balaban P.M. Histone acetylation determines transcription of atypical protein kinases in rat neurons. Scientific Reports. 2019. V. 9. N. 1. P. 4332. DOI: 10.1038/s41598-019-40823-z
- Chesnokova E., Zuzina A., Bal N., Vinarskaya A., Roshchin M., Artyuhov A., Dashinimaev E., Aseyev N., Balaban P., Kolosov P. Experiments with Snails Add to Our Knowledge about the Role of aPKC Subfamily Kinases in Learning. International Journal Of Molecular Sciences. 2019. V. 20. N. 9. P. 2117. DOI: 10.3390/ijms20092117
- Egorov A.V., Schumacher D., Medert R., Birnbaumer L., Freichel M., Draguhn A. TRPC channels are not required for graded persistent activity in entorhinal cortex neurons. Hippocampus. 2019. V. 29. N. 11. P. 1038-1048. DOI: 10.1002/hipo.23094
- Ivanova V.O., Bal N.V., Balaban P.M. Nitric oxide is involved in the mechanism of ampa receptors incorporation into dendrites of pyramidal neurons in hippocampus . // BNA Festival of Neuroscience 2019. 2019. V. 3. PT039 (SP) .
- Johansson N., Anikin A., Aseyev N.A. Color sound symbolism in natural languages. Language and Cognition. 2019. V. 12. N. 1. P. 56-83. DOI: 10.1017/langcog.2019.35
- Kost L.A., Ivanova V.O., Balaban P.M., Lukyanov K.A., Nikitin E.S., Bogdanov A.M. Red Fluorescent Genetically Encoded Voltage Indicators with Millisecond Responsiveness. Sensors (Basel, Switzerland). 2019. V. 19. N. 13. P. 2982. DOI: 10.3390/s19132982
- Maltsev A.V., Bal N.V., Balaban P.M. LTP suppression by protein synthesis inhibitors is NO-dependent. Neuropharmacology. 2019. V. 146. P. 276-288. DOI: 10.1016/j.neuropharm.2018.12.009
- Malyshev A.Y., Balaban P.M. More Light on the Brain: 30 Years Later. Neuroscience and Behavioral Physiology. 2019. V. 49. N. 2. P. 159-162. DOI: 10.1007/s11055-019-00728-w
- Nikitin E.S., Roschin V.Y., Ierusalimsky V.N., Egorov A.V., Balaban P.M. Optogenetic Stimulation of the Axons of Visual Cortex and Hippocampus Pyramidal Neurons in Living Brain Slices. Neuroscience and Behavioral Physiology. 2019. V. 49. N. 2. P. 227-232. DOI: 10.1007/s11055-019-00719-x
- Smirnova G.R., Roshchin M.V., Vinarskaya A.Kh., Kolotova D.Y., Simonova N.A., Balaban P.M., Malyshev A.Y. Use of Anchoring Motifs to Support the Central and Peripheral Locations of Opsins in Optogenetics. Neuroscience and Behavioral Physiology. 2019. V. 49. N. 9. P. 1089-1091. DOI: 10.1007/s11055-019-00843-8
- Tyshkovskiy A., Bozaykut P., Borodinova A.A., Gerashchenko M.V., Ables G.P., Garratt M., Khaitovich P., Clish C.B., Miller R.A., Gladyshev V.N. Identification and Application of Gene Expression Signatures Associated with Lifespan Extension. Cell Metabolism. 2019. V. 30. P. 573-593. DOI: 10.1016/j.cmet.2019.06.018
- Xu C., Li Q., Efimova O., Petrova M., Vinarskaya A.Kh., Kolosov P.M., Aseyev N.A., Koshkareva K., Ierusalimsky V.N., Balaban P.M., Khaitovich P. Identification of immediate early genes in the nervous system of snail Helix lucorum. eNeuro. 2019. ENEURO.0416-18.2019. DOI: 10.1523/ENEURO.0416-18.2019
- Blagirev A.A., Chesnokova E.A., Bal N.V., Kolosov P.M. Single neuron transcriptomics. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I.P. Pavlova. 2018. V. 68. N. 6. P. 675-702. DOI: 10.1134/S0044467718060047
- Dobryakova Y.V., Kasianov A., Zaichenko M.I., Stepanichev M.Y., Chesnokova E.A., Kolosov P.M., Markevich V.A., Bolshakov A.P. Intracerebroventricular administration of <sup>192</sup>IgG-saporin alters expression of microglia-associated genes in the dorsal but not ventral hippocampus. Frontiers in Molecular Neuroscience. 2018. V. 10. P. 429. DOI: 10.3389/fnmol.2017.00429
- Doronin D.A., Barykina N.V., Subach O.M., Sotskov V.P., Plusnin V.V., Ivleva O.A., Isaakova E.A., Varizhuk A.M., Pozmogova G.E., Malyshev A.Y., Piatkevich K.D., Anokhin K.V., Enikolopov G.N., Subach F.V. Genetically encoded calcium indicator with NTnC-like design and enhanced fluorescence contrast and kinetics. BMC Biotechnology. 2018. V. 18. N. 1. P. 10. DOI: 10.1186/s12896-018-0417-2
- Ierusalimsky V.N., Balaban P.M. Long-living RNA in the CNS of terrestrial snail. RNA Biology. 2018. V. 15. N. 2. P. 207-213. DOI: 10.1080/15476286.2017.1411460
- Muller P., Draguhn A., Egorov A.V. Persistent sodium current modulates axonal excitability in CA1 pyramidal neurons. Journal Of Neurochemistry. 2018. V. 146. N. 4. P. 446-458. DOI: 10.1111/jnc.14479
- Roshchin M.V., Ermakova Y.G., Lanin A.A., Chebotarev A.S., Kelmanson I.V., Balaban P.M., Zheltikov A.M., Belousov V.V., Nikitin E.S. Thermogenetic stimulation of single neocortical pyramidal neurons transfected with TRPV1-L channels. Neuroscience Letters. 2018. V. 687. P. 153-157. DOI: 10.1016/j.neulet.2018.09.038
- Roshchin M.V., Ierusalimsky N.V., Matlashov M.V., Balaban P.M., Belousov V.V., Kemenes G., Staras K., Nikitin E.S. A BK channel–mediated feedback pathway links single-synapse activity with action potential sharpening in repetitive firing. Science Advances. 2018. V. 4. N. 7. DOI: 10.1126/SCIADV.AAT1357
- Thome C., Roth F.C., Obermayer J., Yanez A., Draguhn A., Egorov A.V. Synaptic entrainment of ectopic action potential generation in hippocampal pyramidal neurons. The Journal Of Physiology. 2018. V. 596. N. 21. P. 5067-5068. DOI: 10.1113/JP276720
- Aseyev N.A., Vinarskaya A.K., Roshchin M., Korshunova T.A., Malyshev A.Y., Zuzina A.B., Ierusalimsky V.N., Lemak M.S., Zakharov I.S., Kolosov P.M., Chesnokova E.A., Volkova S., Kasianov A., Uroshlev L., Popova Y., Boyle R.D., Balaban P.M. Adaptive changes in the vestibular system of land snail to a 30-day spaceflight and readaptation on return to earth. Frontiers in Cellular Neuroscience. 2017. V. 11. P. 348. DOI: 10.3389/fncel.2017.00348
- Bal N.V., Roshchin M., Salozhin S., Balaban P.M. Nitric Oxide Upregulates Proteasomal Protein Degradation in Neurons. Cellular and Molecular Neurobiology. 2017. V. 37. N. 5. P. 763-769. DOI: 10.1007/s10571-016-0413-9
- Bal N.V., Rysakova M.P., Vinarskaya A.K., Ivanova V.O., Zuzina A.B., Balaban P.M. Cued memory reconsolidation in rats requires nitric oxide. European Journal of Neuroscience. 2017. V. 45. N. 5. P. 643-647. DOI: 10.1111/ejn.13503
- Barykina N.V., Subach O.M., Piatkevich K.D., Jung E.E., Malyshev A.Y., Bogorodskiy A.O., Borshchevskiy V.I., Varizhuk A.M., Pozmogova G.E., Boyden E.S., Anokhin K.V., Enikolopov G.N., Subach F.V. Green fluorescent genetically encoded calcium indicator based on calmodulin/M13-peptide from fungi. PLoS ONE. 2017. V. 12. N. 8. e0183757. DOI: 10.1371/journal.pone.0183757
- Bogodvid T.K., Andrianov V.V., Deryabina I.B., Muranova L.N., Silantyeva D.I., Vinarskaya A., Balaban P.M., Gainutdinov K.L. Responses of withdrawal interneurons to serotonin applications in naïve and learned snails are different. Frontiers in Cellular Neuroscience. 2017. V. 11. P. 403. DOI: 10.3389/fncel.2017.00403
- Borodinova A.A., Zuzina A.B., Balaban P.M. Role of atypical protein kinases in maintenance of long-term memory and synaptic plasticity. Biochemistry (Moscow). 2017. V. 82. N. 3. P. 243-256. DOI: 10.1134/S0006297917030026
- Chesnokova E.A., Bal N.V., Kolosov P.M. Kinases of eIF2a switch translation of mRNA subset during neuronal plasticity. International Journal of Molecular Sciences. 2017. V. 18. N. 10. E2213. DOI: 10.3390/ijms18102213
- Ermakova Y.G., Lanin A.A., Fedotov I.V., Roshchin M., Kelmanson I.V., Kulik D., Bogdanova Y.A., Shokhina A.G., Bilan D.S., Staroverov D.B., Balaban P.M., Fedotov A.B., Sidorov-Biryukov D.A., Nikitin E.S., Zheltikov A.M., Belousov V.V. Thermogenetic neurostimulation with single-cell resolution. Nature Communications. 2017. V. 8. P. 15362. DOI: 10.1038/ncomms15362
- Kost L.A., Nikitin E.S., Ivanova V.O., Sung U., Putintseva E.V., Chudakov D.M., Balaban P.M., Lukyanov K.A., Bogdanov A.M. Insertion of the voltage-sensitive domain into circularly permuted red fluorescent protein as a design for genetically encoded voltage sensor. PLoS ONE. 2017. V. 12. N. 9. e0184225. DOI: 10.1371/journal.pone.0184225
- Malyshev A.Y., Roshchin M.V., Smirnova G.R., Dolgikh G.A., Balaban P.M., Ostrovsky M.A. Chloride conducting light activated channel GtACR2 can produce both cessation of firing and generation of action potentials in cortical neurons in response to light. Neuroscience Letter. 2017. V. 640. P. 76-80.
- Nikitin E.S., Bal N.V., Malyshev A.Y., Ierusalimsky V.N., Spivak Y.S., Balaban P.M., Volgushev M.A. Encoding of high frequencies improves with maturation of action potential generation in cultured neocortical neurons. Frontiers in Cellular Neuroscience. 2017. V. 11. P. 28. DOI: 10.3389/fncel.2017.00028
- Nikitin E.S., Roschin V.Y., Ierusalimsky V.N., Egorov A.V., Balaban P.M. Optogenetic stimulation of axons of pyramidal neurons in acute brain slices of the visual cortex and hippocampus. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I.P. Pavlova. 2017. V. 67. N. 5. P. 101-108. DOI: 10.7868/S0044467717050112
- Balaban P.M. Comparative Physiology of Memory. Aktualnyje Voprosy Sovremennoj Fiziologii. 2016. V. 1. P. 87-101.
- Dolgikh D.A., Malyshev A.Y., Roshchin M.V., Smirnova G.R., Nekrasova O.V., Petrovskaya L.E., Feldman T.B., Balaban P.M., Kirpichnikov M.P., Ostrovsky M.A. Comparative characteristics of two anion-channel rhodopsins and prospects of their use in optogenetics. Doklady Biochemistry and Biophysics. 2016. V. 471. N. 1. P. 440-442. DOI: 10.1134/S160767291606017X
- Nikitin E.S., Malyshev A.Y., Balaban P.M., Volgushev M.A. Physiological Aspects of the Application of Hodgkin–Huxley Model of Action Potential Initiation for Invertebrate and Vertebrate Neurons. Zhurnal Vysshei Nervnoi Deiatelnosti im I P Pavlova. 2016. V. 66. N. 3. P. 279-288. DOI: 10.7868/S0044467716030084
- Nikitin E.S., Malyshev A.Y., Balaban P.M., Volgushev M.A. Physiological aspects of the use of the Hodgkin – Huxley action potential generation model for invertebrate and vertebrate animals. Zhurnal Vysshei Nervnoi Deiatelnosti im I P Pavlova. 2016. V. 66. N. 3. P. 279-288.
- Chesnokova E.A., Kolosov P.M. Local protein synthesis in dendrites and its regulation normally and during plastic changes. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I.P. Pavlova. 2016. V. 66. N. 2. P. 163-180. DOI: 10.7868/S0044467716010056
- Bal N.V., Malyshev A.Y., Smirnov I., Balaban P.M. Expression of Channelrhodopsin-2 Using in Suspension Electroporation for Studying the Monosynaptic Transmission in Neuronal Culture. BioNanoScience. 2016. V. 6. N. 4. P. 329-331. DOI: 10.1007/s12668-016-0228-7
- Bal N.V., Susorov D., Chesnokova E.A., Kasianov A., Mikhailova E.S., Alkalaeva E., Balaban P.M., Kolosov P.M. Upstream open reading frames located in the leader of protein kinase mζ mRNA regulate its translation. Frontiers in Molecular Neuroscience. 2016. V. 9. P. 103. DOI: 10.3389/fnmol.2016.00103
- Bal N.V., Susorov D., Chesnokova E.A., Kasianov A., Mikhailova T., Alkalaeva E., Balaban P.M., Kolosov P.M. Upstream open reading frames located in the leader of protein kinase mζ mRNA regulate its translation. Frontiers in Molecular Neuroscience. 2016. V. 9. N. OCT2016. P. 103. DOI: 10.3389/fnmol.2016.00103
- Balaban P.M., Vinarskaya A.K., Zuzina A.B., Ierusalimsky V.N., Malyshev A.Y. Impairment of the serotonergic neurons underlying reinforcement elicits extinction of the repeatedly reactivated context memory. Scientific Reports. 2016. V. 6. P. 36933. DOI: 10.1038/srep36933
- Barykina N.V., Subach O.M., Doronin D.A., Sotskov V.P., Roshchina M.A., Kunitsyna T.A., Malyshev A.Y., Smirnov I.V., Azieva A.M., Sokolov I.S., Piatkevich K.D., Burtsev M.S., Varizhuk A.M., Pozmogova G.E., Anokhin K.V., Subach F.V., Enikolopov G.N. A new design for a green calcium indicator with a smaller size and a reduced number of calcium-binding sites. Scientific Reports. 2016. V. 6. P. 34447. DOI: 10.1038/srep34447
- Deryabina I.B., Andrianov V.V., Bogodvid T.K., Muranova L.N., Vinarskaya A.K., Gainutdinov K.L. Serotonin Application Effects on Electrical Characteristics of the Premotor Interneurons in Intact and Trained Snails. BioNanoScience. 2016. V. 6. N. 4. P. 269-271. DOI: 10.1007/s12668-016-0224-y
- Dolgikh D.A., Malyshev A.Y., Roshchin M.V., Smirnova G.R., Nekrasova O.V., Petrovskaya L.E., Feldman T.B., Balaban P.M., Kirpichnikov M.P., Ostrovsky M.A. Comparative characteristics of two anion-channel rhodopsins and prospects of their use in optogenetics. Doklady Biochemistry and Biophysics. 2016. V. 471. N. 1. P. 440-442. DOI: 10.1134/S160767291606017X
- Ierusalimsky V.N., Balaban P.M. RNA synthesis and turnover in the molluscan nervous system studied by Click-iT method. Brain Research. 2016. V. 1633. P. 139-148. DOI: 10.1016/j.brainres.2015.12.049
- Roth F.C., Beyer K.M., Both M., Draguhn A., Egorov A.V. Downstream effects of hippocampal sharp wave ripple oscillations on medial entorhinal cortex layer V neurons in vitro. Hippocampus. 2016. V. 26. N. 12. P. 1493-1508. DOI: 10.1002/hipo.22623
- Balaban P.M., Gulyaeva N.V. Neurophilosophy. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I.P. Pavlova. 2015. V. 65. N. 4. P. 498-502. DOI: 10.7868/S0044467715040036
- Bal N.V., Balaban P.M. Ubiquitin-dependent protein degradation is necessary for long-term plasticity and memory. Zhurnal Vysshei Nervnoi Deiatelnosti im I P Pavlova. 2015. V. 32. N. 4. P. 275-284. DOI: 10.7868/S1027813315040044
- Zuzina A.B., Balaban P.M. Extinction and reconsolidation of memory. Zhurnal Vysshei Nervnoi Deiatelnosti im. I.P. Pavlova. 2015. V. 65. N. 5. P. 564-576. DOI: 10.7868/S0044467715050172
- Ierusalimsky V.N., Borodinova A.A., Balaban P.M. Localization of the atypical protein kinase Cζ in the Nervous System of the terrestrial snail Helix. Neyrokhimiya. 2015. V. 32. N. 4. P. 295-301. DOI: 10.7868/S1027813315040093