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
- Stepanichev M.Y., Tishkina A.O., Lazareva N.A., Martianov E.K., Tukhbatova G.R., Kulagina A.O., Salozhin S.V., Gulyaeva N.V. Expression of TrkA and TrkB neurotrophins high affinity receptors in rat hippocampus after intracerebroventricular administration of βA (25-35). Nejrokhimija. 2015. V. 32. N. 1. P. 57-63.
- Andrianov V.V., Bogodvid T.K., Deryabina I.B., Golovchenko A.N., Muranova L.N., Tagirova R.R., Vinarskaya A.K., Gainutdinov K.L. Modulation of defensive reflex conditioning in snails by serotonin. Frontiers in Behavioral Neuroscience. 2015. V. 23. N. 9. P. 279. DOI: 10.3389/fnbeh.2015.00279
- Bal N.V., Balaban P.M. Ubiquitin-dependent protein degradation is necessary for long-term plasticity and memory. Neurochemical Journal. 2015. V. 9. N. 4. P. 237-244. DOI: 10.1134/S1819712415040042
- Balaban P.M., Roshchin M., Timoshenko A.K., Zuzina A.B., Lemak M., Ierusalimsky V.N., Aseyev N.A., Malyshev A.Y. Homolog of protein kinase Mζ maintains context aversive memory and underlying long-term facilitation in terrestrial snail Helix. Frontiers in Cellular Neuroscience. 2015. V. 22. N. 9. P. 222. DOI: 10.3389/fncel.2015.00222
- Dolgikh D.A., Malyshev A.Y., Salozhin S.V., Nekrasova O.V., Petrovskaya L.E., Roshchin M.V., Borodinova A.A., Feldman T.B., Balaban P.M., Kirpichnikov M.P., Ostrovsky M.A. Anion-selective channelrhodopsin expressed in neuronal cell culture and in vivo in murine brain: Light-induced inhibition of generation of action potentials. Doklady Biochemistry and Biophysics. 2015. V. 465. N. 1. P. 424-427. DOI: 10.1134/S160767291506023X
- Ivanov A.D., Tukhbatova G.R., Salozhin S.V., Markevich V.A. NGF but not BDNF overexpression protects hippocampal LTP from beta-amyloid-induced impairment. Neuroscience. 2015. V. 289. P. 114-122. DOI: 10.1016/j.neuroscience.2014.12.063
- Malyshev A.Y., Goz R., LoTurco J.J., Volgushev M.A. Advantages and limitations of the use of optogenetic approach in studying fast-scale spike encoding. PLoS ONE. 2015. V. 10. N. 4. e0122286. DOI: 10.1371/journal.pone.0122286
- Matlashov M.E., Bogdanova Y.A., Ermakova G.V., Mishina N.M., Ermakova Y.G., Nikitin E.S., Balaban P.M., Okabe S., Lukyanov S.A., Enikolopov G., Zaraisky A.G., Belousov V.V. Fluorescent ratiometric pH indicator SypHer2: Applications in neuroscience and regenerative biology. Biochimica et Biophysica Acta - General Subjects. 2015. V. 1850. N. 11. P. 2318-2328. DOI: 10.1016/j.bbagen.2015.08.002
- Stepanichev M.Y., Tishkina A.O., Lazareva N.A., Mart'yanova E.K., Tukhbatova G.R., Kulagina A.O., Salozhin S.V., Gulyaeva N.V. The expression of the TrkA and TrkB high-affinity neurotrophin receptors in the rat hippocampus after intracerebroventricular administration of Aβ(25–35). Neurochemical Journal. 2015. V. 9. N. 1. P. 47-53. DOI: 10.1134/S1819712415010110
- Vasilyeva L.N., Badakva A.M., Miller N.V., Zobova L.N., Roschin V.Y., Bondar I.V. Long-term recording of single unit activity and criteria for estimation of stability. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I.P. Pavlova. 2014. V. 64. N. 6. P. 693-701. DOI: 10.7868/S004446771406015X
- Mayorova L.A., Martynova O.V., Balaban P.M., Ivanitsky A.M., Schklovskii V.N. Mismatch negativity and its hemodynamic equivalent (based on fMRI) in research of speech perception in healthy and in speech disorders. Uspehi Fiziologicheskikh Nauk. 2014. V. 45. N. 1. P. 27-43.
- Simonova N.A., Garakh Z.V., Zaitseva Y.S., Schmukler A.B. Neurophysiological mechanisms of visual impairment in schizophrenia. Sotsialnaja i Klinicheskaja Psikhiatrija. 2014. V. 24. N. 1. P. 81-89.
- Balaban P.M., Roshchin M., Timoshenko A.K., Gainutdinov K.L., Bogodvid T.K., Muranova L.N., Zuzina A.B., Korshunova T.A. Nitric oxide is necessary for labilization of a consolidated context memory during reconsolidation in terrestrial snails. European Journal of Neuroscience. 2014. V. 40. N. 6. P. 2963-2970. DOI: 10.1111/ejn.12642
- Bannon N.M., Zhang P., Ilin V., Chistiakova M., Volgushev M.A. Modulation of synaptic transmission by adenosine in layer 2/3 of the rat visual cortex in vitro. Neuroscience. 2014. V. 260. P. 171-184. DOI: 10.1016/j.neuroscience.2013.12.018
- Fischer V., Both M., Draguhn A., Egorov A.V. Choline-mediated modulation of hippocampal sharp wave-ripple complexes in vitro. Journal Of Neurochemistry. 2014. V. 129. N. 5. P. 792-805. DOI: 10.1111/jnc.12693
- Korshunova T.A., Balaban P.M. Nitric oxide is necessary for long-term facilitation of synaptic responses and for development of context memory in terrestrial snails. Neuroscience. 2014. V. 266. P. 127-135. DOI: 10.1016/j.neuroscience.2014.02.004
- Lemak M.S., Voloshanenko O., Draguhn A., Egorov A.V. K<inf>ATP</inf> channels modulate intrinsic firing activity of immature entorhinal cortex layer III neurons. Frontiers in Cellular Neuroscience. 2014. V. 8. N. AUG. P. 255. DOI: 10.3389/fncel.2014.00255
- Stepanichev M., Lazareva N., Tukhbatova G., Salozhin S., Gulyaeva N. Transient disturbances in contextual fear memory induced by Aβ(25-35) in rats are accompanied by cholinergic dysfunction. Behavioural Brain Research. 2014. V. 259. P. 152-157. DOI: 10.1016/j.bbr.2013.11.013
- Stepanichev M.Y., Lazareva N.A., Tukhbatova G.R., Salozhin S., Gulyaeva N.V. Transient disturbances in contextual fear memory induced by Aβ(25-35) in rats are accompanied by cholinergic dysfunction. Behavioural Brain Research. 2014. V. 259. P. 152-157. DOI: 10.1016/j.bbr.2013.11.013
- Thome C., Kelly T., Yanez A., Schultz C., Engelhardt M., Cambridge S.B., Both M., Draguhn A., Beck H., Egorov A.V. Axon-carrying dendrites convey privileged synaptic input in hippocampal neurons. Neuron. 2014. V. 83. N. 6. P. 1231-4. DOI: 10.1016/j.neuron.2014.08.013
- Badakva A.M., Bondar I.V., Zobova L.N., Miller N.V., Roschin V.Y. Modeling an invasive brain - computer interface in an experiment with primates. Aviakosmicheskaja i Ekologicheskaja Medistyna. 2013. V. 47. N. 2. P. 61-64.
- Nikitin E.S., Aseyev N.A., Balaban P.M. Advanced optical recording of neuronal activity with voltage-sensitive dyes. Zhurnal vyssheĭ nervnoĭ deiatelnosti imeni I P Pavlova. 2013. V. 63. N. 6. P. 656-666. DOI: 10.7868/S0044467713060129
- Nikitin E.S., Balaban P.M. Compartmentalization of neral non-synaptic plasticity at subcellular level. Zhurnal vyssheǐ nervnoǐ deiatelnosti imeni I P Pavlova. 2013. V. 63. N. 3. P. 295-302. DOI: 10.7868/S0044467713030076
- Aseyev N.A., Roshchin M., Ierusalimsky V.N., Balaban P.M., Nikitin E.S. Biolistic delivery of voltage-sensitive dyes for fast recording of membrane potential changes in individual neurons in rat brain slices. Journal of Neuroscience Methods. 2013. V. 212. N. 1. P. 17-27. DOI: 10.1016/j.jneumeth.2012.09.008
- Chen J.-., Lonjers P., Lee C., Chistiakova M., Volgushev M.A., Bazhenov M. Heterosynaptic plasticity prevents runaway synaptic dynamics. Journal of Neuroscience. 2013. V. 33. N. 40. P. 15915-15929. DOI: 10.1523/JNEUROSCI.5088-12.2013
- Ierusalimsky V.N., Balaban P.M. Type 1 metalloproteinase is selectively expressed in adult rat brain and can be rapidly up-regulated by kainate. Acta Histochemica. 2013. V. 115. N. 8. P. 816-826. DOI: 10.1016/j.acthis.2013.04.001
- Ierusalimsky V.N., Kuleshova E.P., Balaban P.M. Expression of the type 1 metalloproteinase in the rat hippocampus after the intracerebroventricular injection of β-amyloid peptide (25-35). Acta Neurobiol. Exp. (Wars). 2013. V. 73. N. 4. P. 571-578.
- Ilin V., Malyshev A.Y., Wolf F., Volgushev M.A. Fast computations in cortical ensembles require rapid initiation of action potentials. Journal of Neuroscience. 2013. V. 33. N. 6. P. 2281-2292. DOI: 10.1523/JNEUROSCI.0771-12.2013
- Malyshev A.Y., Tchumatchenko T., Volgushev S., Volgushev M.A. Energy-efficient encoding by shifting spikes in neocortical neurons. European Journal of Neuroscience. 2013. V. 38. N. 8. P. 3181-3188. DOI: 10.1111/ejn.12338
- Nikitin E.S., Balaban P.M., Kemenes G. Nonsynaptic plasticity underlies a compartmentalized increase in synaptic efficacy after classical conditioning. Current Biology. 2013. V. 23. N. 7. P. 614-619. DOI: 10.1016/j.cub.2013.02.048
- Suntsova M., Gogvadze E.V., Salozhin S., Gaifullin N., Eroshkin F., Dmitriev S.E., Martynova N., Kulikov K., Malakhova G., Tukhbatova G., Bolshakov A.P., Ghilarov D., Garazha A., Aliper A., Cantor C.R., Solokhin Y., Roumiantsev S., Balaban P.M., Zhavoronkov A., Buzdin A. Human-specific endogenous retroviral insert serves as an enhancer for the schizophrenia-linked gene PRODH. Proceedings of the National Academy of Sciences of the United States of America. 2013. V. 110. N. 48. P. 19472-19477. DOI: 10.1073/pnas.1318172110
- Suntsova M., Gogvadze E.V., Salozhin S., Gaifullin N., Eroshkin F., Dmitriev S.E., Martynova O.V., Kulikov M.A., Malakhova G., Tukhbatova G., Bolshakov A.P., Ghilarov D., Garazha A., Aliper A., Cantor C.R., Solokhin Y., Roumiantsev S., Balaban P.M., Zhavoronkov A., Buzdin A. Human-specific endogenous retroviral insert serves as an enhancer for the schizophrenia-linked gene PRODH. Proceedings of the National Academy of Sciences of the United States of America. 2013. V. 110. N. 48. P. 19472-19477. DOI: 10.1073/pnas.1318172110
- Aseyev N.A., Nikitin E.S., Roschin M.V., Ierusalimsky V.N., Balaban P.M. Fast and aimed delivery of voltage-sensitive dyes to mammalian brain slices by biolistic techniques. Zhurnal Vysshei Nervnoi Deiatelnosti im I P Pavlova. 2012. V. 62. N. 1. P. 100-107.
- Malyshev A.Y., Balaban P.M. Changes in intracellular calcium concentration during generation of high-amplitude EPSPs in grape snail neurons. Zhurnal Vysshei Nervnoi Deiatelnosti im I P Pavlova. 2012. V. 98. N. 11. P. 1298-1306.
- Huang M., Volgushev M.A., Wolf F. A small fraction of strongly cooperative sodium channels boosts neuronal encoding of high frequencies. PLoS ONE. 2012. V. 7. N. 5. e37629. DOI: 10.1371/journal.pone.0037629
- Kononov A.V., Bal N.V., Zinchenko V.P. Control of spontaneous synchronous Ca<sup>2+</sup> oscillations in hippocampal neurons by GABAergic neurons containing kainate receptors without desensitization. Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology. 2012. V. 6. N. 2. P. 215-220. DOI: 10.1134/S1990747812010072
- Lee C.M., Stoelzel C., Chistiakova M., Volgushev M.A. Heterosynaptic plasticity induced by intracellular tetanization in layer 2/3 pyramidal neurons in rat auditory cortex. Journal of Physiology. 2012. V. 590. N. 10. P. 2253-2271. DOI: 10.1113/jphysiol.2012.228247
- Roshchin M., Balaban P.M. Neural control of olfaction and tentacle movements by serotonin and dopamine in terrestrial snail. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology. 2012. V. 198. N. 2. P. 145-158. DOI: 10.1007/s00359-011-0695-9
- Balaban P.M., Korshunova T.A. Network, cellular and molecular mechanisms of plasticity in simple nervous systems. Uspechi Fiziologicheskikh Nauk. 2011. V. 42. N. 4. P. 3-19.
- Balaban P.M., Roschin M.V., Korshunova T.A. Two-faced nitric oxide is necessary for both erasure and consolidation of memory. Zhurnal Vysshei Nervnoi Deiatelnosti im. I.P. Pavlova. 2011. V. 61. N. 3. P. 274-280.
- Malyshev A.Y., Balaban P.M. The role of mediator dendro-somatic release in interneuronal communication. Rossijskij Fiziologisheskij Zhurnal im I M Sechenova. 2011. V. 97. N. 10. P. 1084-1091.
- Nikitin E.S., Balaban P.M. Functional organization and structure of the serotonergic neuronal network of terrestrial snail. Zhurnal Vysshei Nervnoi Deiatelnosti im I P Pavlova. 2011. V. 61. N. 6. P. 750-762.
- Balaban P.M., Malyshev A.Y., Ierusalimsky V.N., Aseyev N.A., Korshunova T.A., Bravarenko N.I., Lemak M.S., Roshchin M., Zakharov I.S., Popova Y., Boyle R. Functional changes in the snail statocyst system elicited by microgravity. PLoS ONE. 2011. V. 6. N. 3. e17710. DOI: 10.1371/journal.pone.0017710
- Chauvette S., Crochet S., Volgushev M.A., Timofeev I. Properties of slow oscillation during slow-wave sleep and anesthesia in cats. Journal of Neuroscience. 2011. V. 31. N. 42. P. 14998-15008. DOI: 10.1523/JNEUROSCI.2339-11.2011
- Hoch T., Volgushev S., Malyshev A.Y., Obermayer K., Volgushev M.A. Modulation of the amplitude of γ-band activity by stimulus phase enhances signal encoding. European Journal of Neuroscience. 2011. V. 33. N. 7. P. 1223-1239. DOI: 10.1111/j.1460-9568.2011.07593.x
- Ierusalimsky V.N., Balaban P.M. Family of CNP neuropeptides: Common morphology in various invertebrates. Cell and Tissue Research. 2011. V. 343. N. 3. P. 483-497. DOI: 10.1007/s00441-010-1119-9
- Malyshev A.Y., Balaban P.M. Serotonergic cerebral cells control activity of cilia in the foregut of the pteropod mollusk Clione limacina. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology. 2011. V. 197. N. 1. P. 25-32. DOI: 10.1007/s00359-010-0581-x
- Tchumatchenko T., Malyshev A.Y., Wolf F., Volgushev M.A. Ultrafast population encoding by cortical neurons. Journal of Neuroscience. 2011. V. 31. N. 34. P. 12171-12179. DOI: 10.1523/JNEUROSCI.2182-11.2011
- Volgushev M.A., Chauvette S., Timofeev I. Long-range correlation of the membrane potential in neocortical neurons during slow oscillation. Progress in Brain Research. 2011. V. 193. P. 181-199. DOI: 10.1016/B978-0-444-53839-0.00012-0
- Ierusalimsky V.N., Balaban P.M. Serotonergic system of neurons in the CNS of terrestrial snail: morphology, ontogenesis, control of behavior. Zhurnal Vyssnei Nervnoi Deiatelnosti im I P Pavlova. 2010. V. 60. N. 5. P. 515-524.