Neurobiology of Development

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Laboratories

About the Lab

Our lab is guided by the principles of classical neuroethology: we use evolutionary and comparative approach to the study of animal behavior, its ontogenesis and the underlying control by neurons. 

The key hypotheses that our studies are based upon are the following:

  • diversity of neurotransmitters is a key principle of operation of a nervous system, not a functionally unnecessary by-product of evolution;
  • neuron is an endogenously active entity; it cannot be described by the passive input-output function;
  • nervous system (and, most probably, the whole organism) utilizes the principle of predictive coding at every level, in its short-term and long-term activities.

Our preferred invertebrate model organisms allow us to work with single identifiable neurons, to study both the cellular and network properties, and to carry out pharmacological and molecular analyses. In collaboration with the Institute of Control Sciences (RAS) we use discrete mathematical modeling of idealistic and real-life neuronal ensembles to test our hypotheses and to develop new, biologically plausible artificial neural networks.

Lab members

Igor Zakharov

Dmitri Sakharov

Varvara Dyakonova

Ilya Chistopolsky

Dmitry Vorontsov

Dmitry Boguslavky

Tatiana Korshunova

Olga Boyko

Taisia Dyakonova

Maxim Mezheritskiy

Rustem Ilyasov

Igor Zakharov

Head of the Lab, Doctor of Biological Sciences

Selected publications

  • Nikitin E.S., Zakharov I.S., Samarova E.I., Kemenes G., Balaban P.M. 2005. Fine tuning of olfactory orientation behaviour by the interaction of oscillatory and single neuronal activity. Eur. J. Neurosci. V. 11. P. 2833-2844.
  • Aseyev N, Zakharov IS, Balaban PM (2010) Morphology of neuropeptide CNP2 modulation of heart activity in terrestrial snail. Peptides, Vol.31 (7), pp. 1301-1308.
  • Balaban P.M., Malyshev A.Y., Ierusalimsky V.N., Aseyev N., 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. 6(3):e17710.
  • Dyakonova V.E., Hernadi L., Ito E., Dyakonova T.L., Chistopolsky I.A., Zakharov I.S., Sakharov D.A. The activity of isolated neurons and the modulatory state of an isolated nervous system represent a recent behavioural state // J. Exp. Biol. 2015. V. 218(Pt 8). P.1151-1158.

Dmitri Sakharov

Former Head of the Lab, Chief researcher, Doctor of Biological Sciences

Selected publications

  • Sakharov DA, Croll RP, guesting editors (1996) Neurotransmitters: Developmental Aspects. Special issues of "Cellular and Molecular Neurobiology", 16 (5 and 6): pp 529-713.
  • Sakharov DA, Winlow W, eds. (1991) Simpler Nervous Systems. Manchester University Press, 391 pp.
  • Winlow W, Vinogradova OS, Sakharov DA, eds. (1991) Signal Molecules & Behaviour. Manchester University Press, 351 pp.
  • CELLULAR ASPECTS OF INVERTEBRATE NEUROPHARMACOLOGY Sakharov D.A. Annual Review of Pharmacology and Toxicology. 1970. Т. 10. С. 335.
  • EVOLUTIONARY ASPECTS OF TRANSMITTER HETEROGENEITY Sakharov D.A. Journal of Neural Transmission, Supplement. 1974. Т. 11. С. 43.
  • SEROTONIN-CONTAINING CELLS IN THE ASCIDIAN ENDOSTYLE Sakharov D.A., Salimova N. Experientia. 1981. Т. 38. С. 802.
  • DRUG-INDUCED LOCOMOTOR STEREOTYPES IN APLYSIA Sakharov D.A., Milosevic I., Salimova N. Comparative Biochemistry and Physiology. 1989. Т. 93. С. 161.
  • MODE OF ACTION OF ANTIPSYCHOTIC DRUGS: LESSONS FROM SIMPLER MODELS Baker M.W., Croll R.P., Dyakonova V., Khabarova M., Sakharov D.A., Voronezhskaya E. Acta Biologica Hungarica. 1995. Т. 46. С. 221.
  • PLEURAL-BUCCAL INTERNEURONS IN THE PTEROPOD MOLLUSC CLIONE LIMACINA Alania M.A., Sakharov D.A., Panchin Y.V. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology. 1999. Т. 185. № 3. С. 267-275.
  • THE ACTIVITY OF ISOLATED NEURONS AND THE MODULATORY STATE OF AN ISOLATED NERVOUS SYSTEM REPRESENT A RECENT BEHAVIOURAL STATE Dyakonova V.E., Hernadi L., Ito E., Dyakonova T.L., Chistopolsky I.A., Zakharov I.S., Sakharov D.A. J. Exp. Biol. 2015. V. 218(Pt 8). P.1151-1158.
  • Alania M., Sakharov D.A., Elliott C.J.H. 2004. Multilevel inhibition of feeding by a peptidergic pleural interneuron in the mollusc Lymnaea stagnalis. J. Comp Physiol A. V. 190. P. 379-390.

Varvara Dyakonova

Chief researcher, Doctor of Biological Sciences

Varvara graduated from the Faculty of Biology of Moscow State University in 1992 and got her PhD in 1997 at IDB RAS studying opioidergic system in the pond snail Lymnaea stagnalis. Her doctoral thesis (2011) was dedicated to neurotransmitter mechanisms of context-dependent behavior. She is now working in the field of invertebrate neuroethology with primary focus on cellular, neurotransmitter and genetic basis of behavior. Varvara has additional interest in evolution and costs of cognitive functions.

Selected publications

  • Mezheritskiy, M., Vorontsov, D., Lapshin, D. Dyakonova V. (2020) Previous flight facilitates partner finding in female crickets. Sci Rep 10, 22328 https://doi.org/10.1038/s41598-020-78969-w
  • Aonuma H., Mezheritskiy M., Boldyshev B., Totani Y., Vorontsov D., Zakharov I., Ito E., Dyakonova V. The Role of Serotonin in the Influence of Intense Locomotion on the Behavior Under Uncertainty in the Mollusk Lymnaea stagnalis//Frontiers in Physiology. – 2020. – Vol. 11. – N Art. 221. DOI: 10.3389/fphys.2020.00221
  • Totani Y., Nakai J., Dyakonova V.E., Lukowiak K., Sakakibara M., Ito E. Induction of LTM following an Insulin Injection//eNeuro. – 2020. – Vol. 7. – Is. 2. DOI: 10.1523/ENEURO.0088-20.2020. (WoS, Scopus
  • Dyakonova TL, Sultanakhmetov GS, Mezheritskiy MI, Sakharov DA, Dyakonova VE. Storage and erasure of behavioural experiences at the single neuron level. Sci Rep. 2019 Oct 14;9(1):14733. doi: 10.1038/s41598-019-51331-5.
  • A. Korshunova, D. D. Vorontsov, V. E. Dyakonova (2016) Previous motor activity affects transition from uncertainty to decision-making in snails. Journal of Experimental Biology https://doi.org/10.1242/jeb.146837
  • Dyakonova VE, Chistopolsky IA, Dyakonova TL, Vorontsov DD, Sakharov DA. (2009) Direct and decarboxylation-dependent effects of neurotransmitter precursors on firing of isolated monoaminergic neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 195(6):515-27.
  • Stevenson P.A., Dyakonova V.E., Rillich J., Schildberger K. (2005) Octopamine and Experience-Dependent Modulation of Aggression in Crickets. J. Neurosci., 25(6): 1431-1441.
  • Dyakonova V.E. (2001) Role of opioid peptides in behavior of invertebrates. Review. Journal of Evolutionary Biochemistry and Physiology, July 2001, vol. 37, no. 4, pp. 335-347(13)

Ilya Chistopolsky

Researcher, PhD

Selected publications

  • I.A. Chistopol’skii, D.A. Sakharov (2003) Non-Synaptic Integration of the Cell Bodies of Neurons into the Central Nervous System of the Snail. // Neuroscience and Behavioral Physiology, Vol.33. №3. p.295-300
  • I.A. Chistopol’skii (2005) Interaction of neurons at the level of cell bodies in the snail CNS. Heterogeneity of the neuroactive environment. // Neuroscience and Behavioral Physiology. Vol.35. №7. p.737-740.
  • I.A. Chistopolsky, D.D. Vorontsov, D.A. Sakharov (2008) Monitoring of neuroactive factors released from a pattern-generating network. // Acta biologica hungarica, Vol. 59. p.29-31
  • V.E. Dyakonova, I.A. Chistopolsky, T.L. Dyakonova, D.D. Vorontsov, D.A. Sakharov (2009) Direct and decarboxylation-dependent eVects of neurotransmitter precursors on Wring of isolated monoaminergic neurons. // J.Comp.Physiol.A. Vol.195. p.515–527
  • V.E. Dyakonova, L. Hernadi, E. Ito, T.L. Dyakonova, I.A. Chistopolsky, I.S. Zakharov, D.A. Sakharov (2015) The activity of isolated neurons and the modulatory state of an isolated nervous system represent a recent behavioural state // J.Exp.Biol. Vol.218. p.1151-1158 

Dmitry Vorontsov

Senior researcher, PhD

Dmitry graduated from the Faculty of Biology of Moscow State University in 1999 and got his PhD in 2003 at IDB RAS studying coordination of motor programs in the brain of pond snail. He is now working in the field of invertebrate neuroethology with primary focus on behavior and with the theory of predictive coding constantly in mind. Dmitry has additional scientific interest in paleontology.  

Selected publications

  • Lapshin D.N., Vorontsov D.D. (2021) Frequency tuning of swarming male mosquitoes (Aedes communis, Culicidae) and its neural mechanisms.  J. Insect Physiology, 2021, Volume 132, 104233, https://doi.org/10.1016/j.jinsphys.2021.104233
  • Mezheritskiy, M., Vorontsov, D., Lapshin, D. Dyakonova V. (2020) Previous flight facilitates partner finding in female crickets. Sci Rep 10, 22328 https://doi.org/10.1038/s41598-020-78969-w
  • Lapshin D.N., Vorontsov D.D. (2019) Directional and frequency characteristics of auditory neurons in Culex male mosquitoes. Journal of Experimental Biology. v. 222. https://doi.org/10.1242/jeb.208785
  • Sidorchuk E.A., Vorontsov D.D. (2018) Preparation of small-sized 3D amber  samples: state of the technique. Palaeoentomology, 1 (1), 80–90. https://doi.org/10.11646/palaeoentomology.1.1.10
  • A. Korshunova, D. D. Vorontsov, V. E. Dyakonova (2016) Previous motor activity affects transition from uncertainty to decision-making in snails. Journal of Experimental Biology https://doi.org/10.1242/jeb.146837
  • Lapshin D.N., Vorontsov D.D. (2009) The dependence of behavioral auditory thresholds on the delay of echo-like signals in noctuid moths (Lepidoptera, Noctuidae). Journal of Integrative Neuroscience, 2009. V.8:1. P. 1 - 12.
  • Vorontsov D.D., Tsyganov V.V., Sakharov D.A. (2004) Phasic coordination between locomotor and respiratory rhythms in Lymnaea: Real behavior and computer imitation. Acta biol. hung. 55 (1-4): 233-237

Dmitry Boguslavky

Researcher, PhD

Selected publications

  • V. Boguslavsky, I. S. Zakharov. Role of External Factors in Embryogenesis of Apis mellifera. Russian Journal of Developmental Biology, 2021, Vol. 52, No. 6, pp. 432–439. DOI: 10.1134/S1062360421060023
  • Ivanova JL, Leonova OG, Popenko VI, Ierusalimsky VN, Korshunova TA, Boguslavsky DV, Malyshev AY, Balaban PM, Belyavsky AV. Intracellular localization of the HCS2 gene products in identified snail neurons in vivo and in vitro//Cell Mol Neurobiol. 2006 Mar;26(2):127-44.
  • Aseyev N, Ierusalimsky V, Boguslavsky D, Balaban P. Snail peptide expression pattern in the nervous system of the medicinal leech.//Brain Res Mol Brain Res. 2005 Oct 31;140(1-2):99-105.
  • Ierusalimsky VN, Boguslavsky DV, Belyavsky AV, Balaban PM. Helix peptide immunoreactivity pattern in the nervous system of juvenile aplysia //Brain Res Mol Brain Res. 2003 Dec 12;120(1):84-9.
  • Boguslavsky D, Ierusalimsky V, Malyshev A, Balaban P, Belyavsky A. Selective blockade of gene expression in a single identified snail neuron.//Neuroscience. 2003;119(1):15-8.
  • Pivovarov AS, Nistratova VL, Boguslavskii DV. Involvement of Na/Ca exchange and intracellular mobilized Ca2+ in Na,K-pump-mediated control of depression of the cholinosensitivy of common snail neurons [correction of neorons] using a cellular analog of habituation.//Neurosci Behav Physiol. 2003 Feb;33(2):113-21.
  • Pivovarov AS, Boguslavskii DV. The Na,K pump regulates decreases in the cholinosensitivity of neurons in the common snail to a cellular analog of habituation: the role of cellular calcium.//Neurosci Behav Physiol. 2001 Sep-Oct;31(5):539-46. 

Tatiana Korshunova

Senior researcher, PhD

Selected publications

  • Korshunova T.A., Sanamyan N.P., Sanamyan K.E., Bakken T., Lundin K., Fletcher K., Martynov A.V. Biodiversity hotspot in cold waters: a review of the genus Cuthonella with descriptions of seven new species (Mollusca, Nudibranchia)// Contributions to Zoology. 2021. Vol. 90. Is. 2. P. 216-283. 10.1163/18759866-BJA10017
  • Korshunova T.A., Driessen F.M.F., Picton B.E., Martynov A.V. The multilevel organismal diversity approach deciphers difficult to distinguish nudibranch species complex//Scientific Reports. 2021. Vol. 11. Is. 1. Art. no. 18323. 10.1038/s41598-021-94863-5
  • Korshunova T., Fletcher K., Picton B., Lundin K., Kashio S., Sanamyan N., Sanamyan K., Padula V., Schrodl M., Martynov A. The Emperor’s Cadlina, hidden diversity and gill cavity evolution: new insights for the taxonomy and phylogeny of Dorid nudibranchs (Mollusca: Gastropoda)//Zoological Journal of the Linnean Society. – 2020. – V. 189. P. 762-827. https://doi.org/10.1093/zoolinnean/zlz126
  • Korshunova, T., Bakken, T., Grøtan, V. V., Johnson, K. B.; Lundin, K.; Martynov A. A synoptic review of the family Dendronotidae (Mollusca: Nudibranchia): a multilevel organismal diversity approach// Contributions to Zoology. – 2020. – P. 1-61. https://doi.org/10.1163/18759866-bja10014
  • Martynov A., Lundin K., Picton B., Fletcher K., Malmberg K., Korshunova T.2 Multiple paedomorphic lineages of soft-substrate burrowing invertebrates: parallels in the origin of Xenocratena and Xenoturbella//PloS One. – 2020. – Vol. 15. – Is. 1. – P. e0227173. 10.1371/journal.pone.0227173
  • Korshunova, B. Picton, G. Furfaro, P. Mariottini, M. Pontes, J. Prkić, K. Fletcher, K. Malmberg, K. Lundin, A. Martynov (2019) Multilevel fine-scale diversity challenges the ‘cryptic species’ concept.  Scientific reports, Nature Publishing Group (United Kingdom), 9, № 6732, 1-23. https://doi.org/10.1038/s41598-019-42297-5
  • Korshunova T., Lundin K., Malmberg K., Picton B., Martynov A. A. First true brackish-water nudibranch mollusc provides new insights for phylogeny and biogeography and reveals paedomorphosis-driven evolution // PLoS ONE. 13(3), e0192177 https://doi.org/10.1371/journal.pone.0192177
  • Martynov A., Hasegawa K., Korshunova T.A. The Japanese Red Data book marine mollusk Japonacteon nipponensis and a Japonacteon population from Russia belong to the same species: Molecular evidence and recommendations for conservation// Global Ecology and Conservation. 2017. 9: 82–89. https://doi.org/10.1016/j.gecco.2016.12.002
  • Korshunova T.A., Martynov A.V., Bakken T., Picton B.E. External diversity is restrained by internal conservatism: New nudibranch mollusc contributes to the cryptic species problem// Zoologica Scripta. 2017. 46: 683–692. https://doi.org/10.1111/zsc.12253
  • Korshunova T.A., Martynov A.V., Bakken T., Evertsen J., Fletcher K., Mudianta I.W., Saito H., Lundin K., Schredl M., Picton B. Polyphyly of the traditional family Flabellinidae affects a major group of Nudibranchia: aeolidacean taxonomic reassessment with descriptions of several new families, genera, and species (Mollusca, Gastropoda) //ZooKeys. 2017. 717: 1-139. 10.3897/zookeys.717.21885
  • Korshunova T.A., Martynov A.V., Picton B.E. Ontogeny as an important part of integrative taxonomy in tergipedid aeolidaceans (Gastropoda: Nudibranchia) with a descriptionof a new genus and species from the Barents Sea//Zootaxa. 2017. 4324 1: 1–22. https://doi.org/10.11646/zootaxa.4324.1.1
  • Korshunova T., Zimina O., Martynov A., Unique pleuroproctic taxa of the nudibranch family Aeolidiidae from the Atlantic and Pacific Oceans, with description of a new genus and species, Journal of Molluscan Studies, Volume 83, Issue 4, 2017, Pages 409–421, https://doi.org/10.1093/mollus/eyx036
  • Korshunova TA, Vorontsov DD, Dyakonova VE. Previous motor activity affects transition from uncertainty to decision-making in snails. J Exp Biol. 2016 Sep 8. pii: jeb.146837. https://doi.org/10.1242/jeb.146837
  • 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. Apr 25; 266:127-35.  Epub 2014 Feb 19. https://doi.org/10.1016/j.neuroscience.2014.02.004
  • Martynov, A.V., Korshunova, T.A., 2011. Opisthobranch Molluscs of the Seas of Russia. A Colour Guide to their Taxonomy and Biology. Fiton Press, Moscow, 230 pp.

Olga Boyko

Senior researcher, PhD

Selected publications

  • Манухин Б.Н., Бойко О.В. Анализ бета-адренергической реакции амниона куриного эмбриона // ДАН 2000. Т. 374. № 5. С.702-705.
  • Манухин Б.Н., Бойко О.В. Кинетика бета1-адренергической реакции амниона куриного эмбриона // Известия АН. Серия биологическая. 2002. №2. С. 186-191.
  • Бойко О.В., Манухин Б.Н. Фармакологическая характеристика мускариновых холинорецепторов в неиннервированном амнионе куриного эмбриона // ДАН. 2007. Т. 413. №1. С. 120-123.
  • Манухин Б.Н., Бойко О.В. Мускариновые холинорецепторы амниона куриного эмбриона // Известия РАН. Cерия биологическая. 2008. №2. С. 215-222.
  • Бойко О.В., Манухин Б.Н. Значение экстраклеточного Са2+ в сократительных реакциях амниона куриного эмбриона // Онтогенез. 2009. Т. 40, № 4, С. 254-260.
  • Манухин Б.Н., Бердышева Л.В., Бойко О.В., Нестерова Л.А. Общность и различия в действии кокаина на альфа-адренергические и мускариновые реакции // Известия РАН. Cерия биологическая. 2011. № 3. С. 322-333.
  • Бойко О.В., Манухин Б.Н. Внутриклеточная передача холинергического сигнала в амнионе куриного эмбриона // Известия РАН. Cерия биологическая. 2014. № 1. C.1-5. DOI: 10.7868/S0002332914010032 

Taisia Dyakonova

Senior researcher, PhD

Selected publications

  • Dyakonova TL, Sultanakhmetov GS, Mezheritskiy MI, Sakharov DA, Dyakonova VE. Storage and erasure of behavioural experiences at the single neuron level. Sci Rep. 2019 Oct 14;9(1):14733. doi: 10.1038/s41598-019-51331-5.
  • Дьяконова Т.Л. 2002. NO-зависимая регуляция глутаматом активности серотонинергической системы виноградной улитки Helix lucorum. Журн. эвол. биохим. физиол. Т. 38. № 2. С. 156-161.
  • Дьяконова Т.Л. 2003. Перестройка нейрональных взаимодействий при активации разных глутаматных рецепторов. Доклады РАН. Т. 388. № 5. С. 694-700.
  • Dyakonova T.L., Dyakonova V.E. Coordination of rhythm-generating units via NO and extrasynaptic neurotransmitter release. J. Comp. Physiol. A. 2010. V. 196(8). P. 529-541. 

Maxim Mezheritskiy

Junior researcher, PhD

Selected publications

  • Dyakonova T.L., Sultanakhmetov G.S., Mezheritskiy M.I., Sakharov D.A., Dyakonova V.E. Storage and erasure of behavioural experiences at the single neuron level // Scientific reports. 2019. V. 9(1). P. 14733. DOI: 10.1038/s41598-019-51331-5
  • Aonuma H., Mezheritskiy M.1, Boldyshev B., Totani Y., Vorontsov D.1, Zakharov I.1, Ito E., Dyakonova V.1 The Role of Serotonin in the Influence of Intense Locomotion on the Behavior Under Uncertainty in the Mollusk Lymnaea stagnalis//Frontiers in Physiology. – 2020. – Vol. 11. – Art. No 221. DOI: 10.3389/fphys.2020.00221.
  • Mezheritskiy M.1, Vorontsov D.1, Lapshin D., Dyakonova V.1 Previous flight facilitates partner finding in female crickets//Scientific Reports. – 2020. – Vol. 10. – Is. 1. – Art. No 22328. DOI: 10.1038/s41598-020-78969-w.

Rustem Ilyasov

Leading researcher, PhD

Rustem Ilyasov is a head of the Developmental Apiology research group.

Selected Publications

  • Ilyasov RA, Lee ML, Takahashi JI, Kwon HW, Nikolenko AG. A revision of subspecies structure of western honey bee Apis mellifera. Saudi Journal of Biological Sciences. 2020 Dec 1;27(12):3615-21.
  • ILYASOV R, Sooho Lİ, Lee ML, Kwon HW, NİKOLENKO A. Effect of miticides amitraz and fluvalinate on reproduction and productivity of honey bee Apis mellifera. Uludağ Arıcılık Dergisi. 2021 Dec 5;21(1):21-30.
  • Lim S, Jung J, Yunusbaev U, Ilyasov R, Kwon HW. Characterization and its implication of a novel taste receptor detecting nutrients in the honey bee, Apis mellifera. Scientific reports. 2019 Aug 12;9(1):11620.
  • Ilyasov RA, Poskryakov AV, Nikolenko AG. Seven genes of mitochondrial genome enabling differentiation of honeybee subspecies Apis mellifera. Russian Journal of Genetics. 2016 Oct;52:1062-70.
  • Ilyasov RA, Poskryakov AV, Nikolenko AG. New SNP markers of the honeybee vitellogenin gene (Vg) used for identification of subspecies Apis mellifera mellifera L. Russian Journal of Genetics. 2015 Feb;51:163-8.

Collaborations

We constantly seek collaborations in order to provide a multidisciplinary approach to the problems that we study. Currently, our long-term collaborators include

  • research on the mathematical modeling of multi-transmitter neuronal networks, performed together with Prof. Oleg P. Kuznetsov, Dr. Ludmila Zhilyakova and other colleagues from the Institute of Control Sciences, RAS
  • studies of a model sensory system, an auditory organ of mosquito, performed together with Dr. Dmitry N. Lapshin (Institute for Information Transmission Problems, RAS)
  • molecular and ontogenetic searching studies of nudibranch molluscs aimed at finding a new model suitable for cellular and comparative analyses, together with Dr. Alexander V. Martynov (Lomonosov Moscow State University)
  • insect and molluscan genome modifications together with Dr. Yu. Bogdanov (University of Southampton, UK) 
  • mechanisms of context-dependent learning together with Prof. E. Ito (Tokyo University, Japan)