vestnik-bio-msuВестник Московского университета. Серия 16. БиологияVestnik Moskovskogo universiteta. Seriya 16. Biologiya0137-0952Lomonosov Moscow State University, School of Biology10.55959/MSU0137-0952-16-79-2S-5vestnik-bio-msu-1379Research ArticleОБЗОРREVIEWСложные «простые нервные системы»Complex “simple nervous systems”АфанасьеваД. Ю.AfanasyevaD. Yu.

Афанасьева Дарья Юрьевна – лаборант, 117485, г. Москва, Бутлерова, д. 5а;

студент

Butlerova 5a, Moscow, 117485

https://orcid.org/0000-0001-9248-8207БалабанП. М.BalabanP. M.

Балабан Павел Милославович – академик РАН, докт. биол. наук, гл. науч. сотр.,

117485, г. Москва, Бутлерова, д. 5а

Butlerova 5a, Moscow, 117485

pmbalaban@gmail.comИнститут высшей нервной деятельности и нейрофизиологии, Российская академия наук; РНИМУ им. ПироговаРоссияInstitute of Higher Nervous Activity and Neurophysiology, Russian Academy of SciencesRussian FederationИнститут высшей нервной деятельности и нейрофизиологии, Российская академия наукРоссияInstitute of Higher Nervous Activity and Neurophysiology, Russian Academy of SciencesRussian Federation202426082024792S3745Copyright © Афанасьева Д.Ю., Балабан П.М., 20242024Афанасьева Д.Ю., Балабан П.М.Afanasyeva D.Y., Balaban P.M.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://vestnik-bio-msu.elpub.ru/jour/article/view/1379

Наземные брюхоногие моллюски развили новые структуры в нервной системе по сравнению с морскими и водными улитками, чтобы адаптироваться к новой среде обитания. Поведение этих животных качественно отличается от поведения водных брюхоногих моллюсков и включает в себя не только возможность активного взаимодействия с другими животными, но и демонстрацию интереса активным приближением, избегание или бегство в определенных случаях. Феномен «стрелы любви», используемый при оплодотворении, уникален для Природы. У этих животных можно сформировать практически все виды ассоциативной памяти, продемонстрировать консолидацию и реконсолидацию памяти, проанализировать механизмы поддержания и модификации памяти. На уровне функционально идентифицированных нейронов и нейронных кластеров возможно исследовать ассоциативные процессы in vitro, разработана 3-нейронная модель ассоциативных долговременных изменений синаптической эффективности.

Terrestrial gastropods have evolved new structures in the nervous system compared to marine and aquatic snails in order to adapt to their new habitat. The behavior of these animals is qualitatively different from the behavior of aquatic gastropods, includes not only the possibility of active interaction with other animals, but also the demonstration of interest by active approach, avoidance or escape in certain cases. The “arrow of love” used in copulation is unique to Nature. Almost all types of associative memory can be formed in these animals, consolidation and reconsolidation of memory can be demonstrated, and mechanisms of memory maintenance and modification can be analyzed. At the level of functionally identified neurons and neural clusters, it is possible to study associative processes in vitro, a 3-neural model of associative longterm changes in synaptic efficiency has been developed.

нейронсинаптическая пластичностьбеспозвоночныеповедениепамятьреконсолидацияneuronsynaptic plasticityinvertebratesbehaviormemoryreconsolidationReferencesСахаров Д. А. Генеалогия нейронов. Москва: Наука; 1974. 183 с.Сахаров Д. А. Генеалогия нейронов. Москва: Наука; 1974. 183 с.Chase R. Behavior and its neural control in gastropod mollusks. Oxford: Oxford Univ. Press; 2002. 336 pp.Chase R. Behavior and its neural control in gastropod mollusks. Oxford: Oxford Univ. Press; 2002. 336 pp.Zakharov I.S., Hayes N.L., Ierusalimsky V.N., Nowakowski R.S., Balaban P.M. Postembryonic neuronogenesis in the procerebrum of the terrestrial snail, Helix L. J. Neurobiol. 1998;35(3):271–276.Zakharov I.S., Hayes N.L., Ierusalimsky V.N., Nowakowski R.S., Balaban P.M. Postembryonic neuronogenesis in the procerebrum of the terrestrial snail, Helix L. J. Neurobiol. 1998;35(3):271–276.Spallanzani L. Memorie su la respirazione, vol. 1, vol. 2. Milano: Annesio Nobili; 1803. 373 pp.Spallanzani L. Memorie su la respirazione, vol. 1, vol. 2. Milano: Annesio Nobili; 1803. 373 pp.Satoshi W., Kirino Y., Gelperin A. Neural and molecular mechanisms of microcognition in Limax. Learn. Mem. 2008;15(9):633–642.Satoshi W., Kirino Y., Gelperin A. Neural and molecular mechanisms of microcognition in Limax. Learn. Mem. 2008;15(9):633–642.Balaban P.M., Vehovszky A., Maximova O.A., Zakharov I.S. Effect of 5,7-dihydroxytryptamine on the food-aversive conditioning in the snail Helix lucorum L. Brain. Res. 1987;404(1–2):201–210.Balaban P.M., Vehovszky A., Maximova O.A., Zakharov I.S. Effect of 5,7-dihydroxytryptamine on the food-aversive conditioning in the snail Helix lucorum L. Brain. Res. 1987;404(1–2):201–210.Adamo S. A., Chase R. The interactions of courtship, feeding, and locomotion in the behavioral hierarchy of the snail Helix aspersa. Behav. Neur. Biol. 1991;55(1):1–18.Adamo S. A., Chase R. The interactions of courtship, feeding, and locomotion in the behavioral hierarchy of the snail Helix aspersa. Behav. Neur. Biol. 1991;55(1):1–18.Chase R. Brain cells that command sexual behavior in the snail Helix aspersa. J. Neurobiol. 1986;17(6):669–679.Chase R. Brain cells that command sexual behavior in the snail Helix aspersa. J. Neurobiol. 1986;17(6):669–679.Balaban P., Chase R. Stimulation of mesocerebrum in Helix aspersa inhibits the neural network underlying avoidance behavior. J. Compar. Physiol. A. 1990;166(3):421–427.Balaban P., Chase R. Stimulation of mesocerebrum in Helix aspersa inhibits the neural network underlying avoidance behavior. J. Compar. Physiol. A. 1990;166(3):421–427.Willows A.O. Behavioral acts elicited by stimulation of single, identifiable brain cells. Science. 1967;157(3788):570–574.Willows A.O. Behavioral acts elicited by stimulation of single, identifiable brain cells. Science. 1967;157(3788):570–574.Balaban P.M. System of command neurons in snail’s escape behavior. Acta Neurobiol. Exp. 1979;39(2):97–107.Balaban P.M. System of command neurons in snail’s escape behavior. Acta Neurobiol. Exp. 1979;39(2):97–107.Malyshev A.Y., Balaban P.M. Identification of mechanoafferent neurons in terrestrial snail: response properties and synaptic connections. J. Neurophysiol. 2002;87(5):2364–2371.Malyshev A.Y., Balaban P.M. Identification of mechanoafferent neurons in terrestrial snail: response properties and synaptic connections. J. Neurophysiol. 2002;87(5):2364–2371.Balaban P.M., Bravarenko N.I., Maksimova O.A., Nikitin E., Ierusalimsky V.N., and Zakharov I.S. A single serotonergic modulatory cell can mediate reinforcement in the withdrawal network of the terrestrial snail. Neurobiol. Learn. Memory. 2001;75(1):30–50.Balaban P.M., Bravarenko N.I., Maksimova O.A., Nikitin E., Ierusalimsky V.N., and Zakharov I.S. A single serotonergic modulatory cell can mediate reinforcement in the withdrawal network of the terrestrial snail. Neurobiol. Learn. Memory. 2001;75(1):30–50.Balaban P.M. Cellular mechanisms of behavioral plasticity in terrestrial snail. Neurosci. Biobehav. Rev. 2002;26(5):597–630.Balaban P.M. Cellular mechanisms of behavioral plasticity in terrestrial snail. Neurosci. Biobehav. Rev. 2002;26(5):597–630.Никитин Е.С., Балабан П.М. Структурнофункциональная организация сети серотонинергических нейронов наземной улитки. Журн. высш. нервн. деят. им. И.П. Павлова. 2011;61(6):750–762.Никитин Е.С., Балабан П.М. Структурнофункциональная организация сети серотонинергических нейронов наземной улитки. Журн. высш. нервн. деят. им. И.П. Павлова. 2011;61(6):750–762.Kupfermann I., Weiss K. The command neuron concept. Behav. Brain. Sci.1978;1(1):3–39.Kupfermann I., Weiss K. The command neuron concept. Behav. Brain. Sci.1978;1(1):3–39.Kupfermann I., Weiss K. Motor program selection in simple model systems. Current Opin. Neurobiol. 2001;11(6):673–677.Kupfermann I., Weiss K. Motor program selection in simple model systems. Current Opin. Neurobiol. 2001;11(6):673–677.Vehovszky A.L., Elekes H., Balaban P. Serotonergic input on identified command neurons in Helix. Acta. Biol. Hungarica. 1993;44(1):97–101.Vehovszky A.L., Elekes H., Balaban P. Serotonergic input on identified command neurons in Helix. Acta. Biol. Hungarica. 1993;44(1):97–101.Zakharov I.S., Ierusalimsky V.N., Balaban P.M. Pedal serotonergic neurons modulate the synaptic input of withdrawal interneurons of Helix. Invertebrate Neurosci. 1995;1(1):41–52.Zakharov I.S., Ierusalimsky V.N., Balaban P.M. Pedal serotonergic neurons modulate the synaptic input of withdrawal interneurons of Helix. Invertebrate Neurosci. 1995;1(1):41–52.Hawkins R.D., Son H., Arancio O. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Progress Brain Res. 1998;118:155–172.Hawkins R.D., Son H., Arancio O. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Progress Brain Res. 1998;118:155–172.Colwill R.M., Absher R. A., Roberts M.L. Context-US learning in Aplysia Californica. J. Neurosci. 1988;8(12):4434–4439.Colwill R.M., Absher R. A., Roberts M.L. Context-US learning in Aplysia Californica. J. Neurosci. 1988;8(12):4434–4439.Balaban P., Bravarenko N. Long-term sensitization and environmental conditioning in terrestrial snails. Exp. Brain Res. 1993;96(3):487–493.Balaban P., Bravarenko N. Long-term sensitization and environmental conditioning in terrestrial snails. Exp. Brain Res. 1993;96(3):487–493.Sahley C.L., Martin K.A. Analysis of associative learning in the terrestrial mollusc Limax maximus. II. Appetitive learning. J. Comp. Physiol. A, Sens. Neur. Behav. Physiol. 1990;167(3):339–345.Sahley C.L., Martin K.A. Analysis of associative learning in the terrestrial mollusc Limax maximus. II. Appetitive learning. J. Comp. Physiol. A, Sens. Neur. Behav. Physiol. 1990;167(3):339–345.Balaban P.M., Chase R. Self-stimulation in snails. Neurosci. Res. Com. 1989;4(3):139–143.Balaban P.M., Chase R. Self-stimulation in snails. Neurosci. Res. Com. 1989;4(3):139–143.Gainutdinova T.H., Tagirova R.R, Ismailova A.I., Muranova L.N., Samarova E.I., Gainutdinov K.L., Balaban P.M. Reconsolidation of a context long-term memory in the terrestrial snail requires protein synthesis. Learn. Mem. 2005;12(6):620–625.Gainutdinova T.H., Tagirova R.R, Ismailova A.I., Muranova L.N., Samarova E.I., Gainutdinov K.L., Balaban P.M. Reconsolidation of a context long-term memory in the terrestrial snail requires protein synthesis. Learn. Mem. 2005;12(6):620–625.Balaban P., Chase R. Interrelationships of the emotionally positive and negative regions of the brain of the edible snail. Neurosci. Behav. Physiol. 1991;21(2):172–180.Balaban P., Chase R. Interrelationships of the emotionally positive and negative regions of the brain of the edible snail. Neurosci. Behav. Physiol. 1991;21(2):172–180.Balaban P. Behavioral neurobiology of learning in terrestrial snails. Progress Neurobiol. 1993;41(1):1–19.Balaban P. Behavioral neurobiology of learning in terrestrial snails. Progress Neurobiol. 1993;41(1):1–19.Иерусалимский В.H., Захаров И.С., Балабан П.М. Сравнение серотонин-и дофаминергической нейронных систем у половозрелых и ювенильных наземных моллюсков Helix и Eobania. Журн. высш. нервн. деят. им. И.П. Павлова. 1997;47(3):563–576.Иерусалимский В.H., Захаров И.С., Балабан П.М. Сравнение серотонин-и дофаминергической нейронных систем у половозрелых и ювенильных наземных моллюсков Helix и Eobania. Журн. высш. нервн. деят. им. И.П. Павлова. 1997;47(3):563–576.Balaban P.M., Korshunova T.A., Bravarenko N.I. Postsynaptic calcium contributes to reinforcement in a three-neuron network exhibiting associative plasticity. Eur. J. Neurosci. 2004;19(2):227–233.Balaban P.M., Korshunova T.A., Bravarenko N.I. Postsynaptic calcium contributes to reinforcement in a three-neuron network exhibiting associative plasticity. Eur. J. Neurosci. 2004;19(2):227–233.Glanzman D.L., Mackey S.L., Hawkins R.D., Dyke A.M., Lloyd P.E., Kandel E.R. Depletion of serotonin in the nervous system of aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by Tail Shock. J. Neurosci. 1989;9(12):4200–4213.Glanzman D.L., Mackey S.L., Hawkins R.D., Dyke A.M., Lloyd P.E., Kandel E.R. Depletion of serotonin in the nervous system of aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by Tail Shock. J. Neurosci. 1989;9(12):4200–4213.Hammer M., Menzel R. Learning and memory in the honeybee. J. Neurosci. 1995;15(3 Pt. 1):1617–1630.Hammer M., Menzel R. Learning and memory in the honeybee. J. Neurosci. 1995;15(3 Pt. 1):1617–1630.Balaban P.M., Vinarskaya A.K., Zuzina A.B., Ierusalimsky V.N., A. Y. Malyshev A.Y. Impairment of the serotonergic neurons underlying reinforcement elicits extinction of the repeatedly reactivated context memory. Sci. Rep. 2016;6(1):36933.Balaban P.M., Vinarskaya A.K., Zuzina A.B., Ierusalimsky V.N., A. Y. Malyshev A.Y. Impairment of the serotonergic neurons underlying reinforcement elicits extinction of the repeatedly reactivated context memory. Sci. Rep. 2016;6(1):36933.

The authors declare that there are no conflicts of interest present.