I.P. Pavlov Journal of Higher Nervous ActivityI.P. Pavlov Journal of Higher Nervous ActivityЖурнал высшей нервной деятельности им. И.П. Павлова0044-46773034-5316The Russian Academy of Sciences68090210.31857/S0044467725020046ОБЗОРЫ И ТЕОРЕТИЧЕСКИЕ СТАТЬИResearch ArticlePlasticity of the primary visual cortex and mechanisms of perceptual learningПластичность первичной зрительной коры и механизмы перцептивного обученияSmirnovI. V.СмирновИ. В.
Russian Federation
malyshev@ihna.ruMalyshevA. Yu.МалышевА. Ю.
Russian Federation
malyshev@ihna.ruInstitute of Higher Nervous Activity and Neurophysiology of the Russian Academy of SciencesИнститут высшей нервной деятельности и нейрофизиологии Российской академии наук1503202575218920528052025Copyright ©; 2025, Russian Academy of SciencesCopyright ©; 2025, Российская академия наук2025Russian Academy of SciencesРоссийская академия наукhttps://innoscience.ru/0044-4677/article/view/680902

The review explores current insights into the cellular and molecular mechanisms of visual perceptual learning. It provides evidences that perceptual learning is underlaid by long-term synaptic plasticity occurring within the neural networks of the primary visual cortex. Key models of perceptual learning in animals, including stimulus-dependent plasticity and reinforcement learning, are analyzed. Furthermore, the review provides a rationale for the use of the visual cortex, particularly in rodents, as a convenient model for investigating general mechanisms of learning and memory in vivo. Using this approach, the role of homo- and heterosynaptic plasticity in long-term modifications of sensory responses in the visual cortex was convincingly demonstrated. The data obtained on the model of plasticity of visual responses can be extrapolated to general mechanisms of learning and memory, including those beyond perceptual learning.

В обзоре рассматриваются современные представления о клеточных и молекулярных механизмах зрительного перцептивного обучения. Приводятся данные, свидетельствующие о том, что в основе перцептивного обучения лежит долговременная синаптическая пластичность в нейронных сетях первичной зрительной коры. Обсуждаются современные модели перцептивного обучения на животных, такие как стимул-зависимое обучение и обучение с подкреплением. Кроме того, в обзоре обосновывается использование зрительной коры (в частности, грызунов) в качестве модели для изучения общих механизмов обучения и памяти in vivo. С использованием этого подхода была убедительно продемонстрирована роль гомо- и гетеросинаптической пластичности в долговременных модификациях сенсорных ответов зрительной коры. Данные, полученные на модели пластичности зрительных ответов, могут быть экстраполированы на общие механизмы обучения и памяти, в том числе выходящие за границы только перцептивного обучения.

perceptual learningvisual cortexneuronsynapsesynaptic plasticitylong-term potentiationin vivoперцептивное обучениезрительная коранейронсинапссинаптическая пластичностьдолговременная потенциацияin vivoРоссийский научный фондRussian Science Foundation20-15-00398ПВиноградова О.С. Гиппокамп и память. М.: Наука. 1975. 332 с.Павлов И.П. Полн. собр. соч. М.: Изд-во АН СССР. 1951–1952. 8 т.Смирнов И.В., Малышев А.Ю. Гетеросинаптическая пластичность: термин, обозначающий разные феномены. Журн. высш. нервн. деят. им. И.П.Павлова. 2024. 74(6): 643–656.Соколов Е.Н. Механизмы памяти. М: Изд-во МГУ. 1969. 176 с.Соколов Е.Н. Нейронные механизмы памяти и обучения. М.: Наука. 1981. 140 с.Ahmadi M., McDevitt E.A., Silver M.A., Mednick S.C. Perceptual learning induces changes in early and late visual evoked potentials. Vision Res. 2018. 152: 101–109.Baroncelli L., Sale A., Viegi A., Maya Vetencourt J.F., De Pasquale R., Baldini S., Maffei L. Experience-dependent reactivation of ocular dominance plasticity in the adult visual cortex. Exp. Neurol. 2010. 226(1): 100–109.Bear M.F., Singer W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature. 1986. 320(6058): 172–176.Bravarenko N.I., Gusev P. V, Balaban P.M., Voronin L.L. Postsynaptic induction of long-term synaptic facilitation in snail central neurones. Neuroreport. 1995. 6(8): 1182–1186.Brown W.M., Bäcker A. Optimal neuronal tuning for finite stimulus spaces. Neural Comput. 2006. 18(7): 1511–1526.Chen J.-Y., Lonjers P., Lee C., Chistiakova M., Volgushev M., Bazhenov M. Heterosynaptic plasticity prevents runaway synaptic dynamics. J. Neurosci. 2013. 33(40): 15915–15929.Chistiakova M., Bannon N.M., Bazhenov M., Volgushev M. Heterosynaptic plasticity: Multiple mechanisms and multiple roles. Neuroscientist. 2014. 20(5): 483–98.Chistiakova M., Bannon N.M., Chen J.-Y., Bazhenov M., Volgushev M. Homeostatic role of heterosynaptic plasticity: models and experiments. Front. Comput. Neurosci. 2015. 9 89.Chistiakova M., Ilin V., Roshchin M., Bannon X.N., Malyshev A., Kisvárday Z., Volgushev M., Bannon N., Malyshev A., Kisvárday Z., Volgushev M. Distinct Heterosynaptic Plasticity in Fast Spiking and Non-Fast-Spiking Inhibitory Neurons in Rat Visual Cortex. J. Neurosci. 2019. 39(35): 6865–6878.Christofi G., Nowicky A. V, Bolsover S.R., Bindman L.J. The postsynaptic induction of nonassociative long-term depression of excitatory synaptic transmission in rat hippocampal slices. J. Neurophysiol. 1993. 69(1): 219–229.Cooke S.F., Bear M.F. Visual Experience Induces Long-Term Potentiation in the Primary Visual Cortex. J. Neurosci. 2010. 30(48): 16304–16313.Cooke S.F., Komorowski R.W., Kaplan E.S., Gavornik J.P., Bear M.F. Visual recognition memory, manifested as long-term habituation, requires synaptic plasticity in V1. Nat. Neurosci. 2015. 18(2): 262–271.Debanne D., Shulz D.E., Fregnac Y. Temporal constraints in associative synaptic plasticity in hippocampus and neocortex. Can. J. Physiol. Pharmacol. 1995. 73(9): 1295–1311.Debanne D., Shulz D.E., Frégnac Y. Activity-dependent regulation of “on” and “off” responses in cat visual cortical receptive fields. J. Physiol. 1998. 508(2): 523–548.Delgado J.Y., Gómez-González J.F., Desai N.S. Pyramidal Neuron Conductance State Gates Spike-Timing-Dependent Plasticity. J Neurosci. 2010. 30(47):15713–25.El-Boustani S., Ip J.P.K.K., Breton-Provencher V., Knott G.W., Okuno H., Bito H., Sur M. Locally coordinated synaptic plasticity of visual cortex neurons in vivo. Science. 2018. 360(6395): 1349–1354.Espadas-Alvarez A.J., Bannon M.J., Orozco-Barrios C.E., Escobedo-Sanchez L., Ayala-Davila J., Reyes-Corona D., Soto-Rodriguez G., Escamilla-Rivera V., De Vizcaya-Ruiz A., Eugenia Gutierrez-Castillo M., Padilla-Viveros A., Martinez-Fong D. Regulation of human GDNF gene expression in nigral dopaminergic neurons using a new doxycycline-regulated NTS-polyplex nanoparticle system. Nanomedicine Nanotechnology, Biol. Med. 2017. 13(4): 1363–1375.Espinosa J.S., Stryker M.P. Development and Plasticity of the Primary Visual Cortex. Neuron. 2012. 75(2): 230–49.Eysel U.T., Eyding D., Schweigart G. Repetitive optical stimulation elicits fast receptive field changes in mature visual cortex. Neuroreport. 1998. 9(5): 949–954.Fong M.F., Finnie P.S.B., Kim T., Thomazeau A., Kaplan E.S., Cooke S.F., Bear M.F. Distinct laminar requirements for nmda receptors in experience-dependent visual cortical plasticity. Cereb. Cortex. 2020. 30(4): 2555–2572.Frégnac Y., Pananceau M., René A., Huguet N., Marre O., Levy M., Shulz D.E. A re-examination of Hebbian-covariance rules and spike timing-dependent plasticity in cat visual cortex in vivo. Front. Synaptic Neurosci. 2010. 2: 1–21.Frégnac Y., Shulz D., Thorpe S., Bienenstock E. A cellular analogue of visual cortical plasticity. Nature. 1988. 333 (6171): 367–370.Frenkel M.Y., Sawtell N.B., Diogo A.C.M., Yoon B., Neve R.L., Bear M.F. Instructive Effect of Visual Experience in Mouse Visual Cortex. Neuron. 2006. 51 (3): 339–349.Gilbert C.D., Li W. Adult Visual Cortical Plasticity. Neuron. 2012. 75(2): 250–64.Gu Q., Singer W. Involvement of Serotonin in Developmental Plasticity of Kitten Visual Cortex. Eur. J. Neurosci. 1995. 7(6): 1146–1153.Harauzov A., Spolidoro M., DiCristo G., De Pasquale R., Cancedda L., Pizzorusso T., Viegi A., Berardi N., Maffei L. Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J. Neurosci. 2010. 30(1): 361–371.Hebb D.O. The organization of behavior. N.Y.: John Wiley and Sons, Inc. 1949. 335 p.Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 2005. 6(11): 877–888.Hubel D.H., Wiesel T.N. Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J. Neurophysiol. 1963. 26: 994–1002.Huberman A.D., Niell C.M. What can mice tell us about how vision works? Trends Neurosci. 2011. 34(9): 464–473.Idzhilova O.S., Smirnova G.R., Petrovskaya L.E., Kolotova D.A., Ostrovsky M.A., Malyshev A.Y. Cationic channelrhodopsin from the alga platymonas subcordiformis as a promising optogenetic tool. Biochemistry. (Mosc). 2022. 87(11): 1327–1334.Jehee J.F.M., Ling S., Swisher J.D., van Bergen R.S., Tong F. Perceptual Learning Selectively Refines Orientation Representations in Early Visual Cortex. J. Neurosci. 2012. 32(47): 16747.Jeong Y., Cho H.-Y., Kim M., Oh J.-P., Kang M.S., Yoo M., Lee H.-S., Han J.-H. Synaptic plasticity-dependent competition rule influences memory formation. Nat. Commun. 2021. 12(1): 3915.Jia K., Zamboni E., Kemper V., Rua C., Reis Goncalves N., Ka Tsun Ng A., Rodgers C.T., Williams G., Goebel R., Kourtzi Z. Article Recurrent Processing Drives Perceptual Plasticity. Curr. Biol. 2020. 30 4177–4187.e4.Kasamatsu T., Pettigrew J.D. Depletion of Brain Catecholamines: Failure of Ocular Dominance Shift After Monocular Occlusion in Kittens. Science (80-. ). 1976. 194(4261): 206–209.Kuhnt U., Kleschevnikov A.M., Voronin L.L. Long term enhancement of synaptic transmission in the hippocampus after tetanization of single neurons by short intracellular current pulses. Neurosci. Res. Commun. 1994. 14(2): 115–123.Kuo M.C., Dringenberg H.C. Short-term (2 to 5 h) dark exposure lowers long-term potentiation (LTP) induction threshold in rat primary visual cortex. Brain Res. 2009. 1276 58–66.Levi D.M., Li R.W. Perceptual learning as a potential treatment for amblyopia: A mini-review. Vision Res. 2009. 49(21): 2535–2549.Li W., Piëch V., Gilbert C.D. Learning to Link Visual Contours. Neuron. 2008. 57(3): 442–451.Lynch G.S., Dunwiddie T., Gribkoff V. Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature. 1977. 266(5604): 737–739.Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron. 2004. 44(1): 5–21.Malyshev A., Bravarenko N., Balaban P. Dependence of synaptic facilitation postsynaptically induced in snail neurones on season and serotonin level. Neuroreport. 1997. 8(5): 1179–1182.Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 2000. 23: 649–711.Maurer D. Visual development. The Cambridge Handbook of Infant Development: Brain, Behavior, and Cultural Context. 2020. 157–185Maya Vetencourt J.F., Sale A., Viegi A., Baroncelli L., De Pasquale R., O’Leary O.F., Castrén E., Maffei L. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science. 2008. 320(5874): 385–388.McLean J., Palmer L.A. Plasticity of neuronal response properties in adult cat striate cortex. Vis. Neurosci. 1998. 15(1): 177–196.Meliza C.D., Dan Y. Receptive-Field Modification in Rat Visual Cortex Induced by Paired Visual Stimulation and Single-Cell Spiking. Neuron. 2006. 49 (2): 183–189.Miller K.D. Synaptic economics: competition and cooperation in synaptic plasticity. Neuron. 1996. 17(3): 371–374.Milner P. A brief history of the Hebbian learning rule. Can. Psychol. 2003. 44(1): 5–9.Montemurro M.A., Panzeri S. Optimal tuning widths in population coding of periodic variables. Neural Comput. 2006. 18(7): 1555–1576.Montgomery D.P., Hayden D.J., Chaloner F.A., Cooke S.F., Bear M.F. Stimulus-Selective Response Plasticity in Primary Visual Cortex: Progress and Puzzles. Front Neural Circuits. 2022. 15:815554.Morishita H., Miwa J.M., Heintz N., Hensch T.K. Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science. 2010. 330(6008): 1238–1240.Pawlak V., Greenberg D.S., Sprekeler H., Gerstner W., Kerr J.N.D. Changing the responses of cortical neurons from sub- to suprathreshold using single spikes in vivo. Elife. 2013. 2 e00012.Poort J., Khan A.G., Pachitariu M., Nemri A., Orsolic I., Krupic J., Bauza M., Sahani M., Keller G.B., Mrsic-Flogel T.D., Hofer S.B. Learning Enhances Sensory and Multiple Non-sensory Representations in Primary Visual Cortex. Neuron. 2015. 86(6): 1478–1490.Poort J., Wilmes K.A., Blot A., Chadwick A., Sahani M., Clopath C., Mrsic-Flogel T.D., Hofer S.B., Khan A.G. Learning and attention increase visual response selectivity through distinct mechanisms. Neuron. 2022. 110(4): 686–697.e6.Pourtois G., Rauss K.S., Vuilleumier P., Schwartz S. Effects of perceptual learning on primary visual cortex activity in humans. Vision Res. 2008. 48(1): 55–62.Priebe N.J., McGee A.W. Mouse vision as a gateway for understanding how experience shapes neural circuits. Front Neural Circuits. 2014. 8:123.Prusky G.T., West P.W.R., Douglas R.M. Behavioral assessment of visual acuity in mice and rats. Vision Res. 2000. 40(16): 2201–2209.Raiguel S., Vogels R., Mysore S.G., Orban G.A. Learning to see the difference specifically alters the most informative V4 neurons. J. Neurosci. 2006. 26(24): 6589–6602.Rossi L.F., Harris K.D., Carandini M. Spatial connectivity matches direction selectivity in visual cortex. Nature. 2020. 588(7839): 648–652.Sale A., De Pasquale R., Bonaccorsi J., Pietra G., Olivieri D., Berardi N., Maffei L. Visual perceptual learning induces long-term potentiation in the visual cortex. Neuroscience. 2011. 172: 219–225.Schoups A., Vogels R., Qian N., Orban G. Practising orientation identification improves orientation coding in V1 neurons. Nature. 2001. 412(6846): 549–553.Seitz A.R. Perceptual learning. Curr. Biol. 2017. 27(13): 631–636.Shouval H.Z., Wang S.S.H., Wittenberg G.M. Spike timing dependent plasticity: A consequence of more fundamental learning rules. Front. Comput. Neurosci. 2010. 4 1601.Simonova N.A., Volgushev M.A., Malyshev A.Y. Enhanced Non-Associative Long-Term Potentiation in Immature Granule Cells in the Dentate Gyrus of Adult Rats. Front. Synaptic Neurosci. 2022. 14 889947.Sjöström P.J., Turrigiano G.G., Nelson S.B. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron. 2001. 32(6): 1149–1164.Smirnov I. V, Malyshev A.Y. Paired optogenetic and visual stimulation can change the orientation selectivity of visual cortex neurons. Biochem. Biophys. Res. Commun. 2023. 646 63–69.Smirnov I. V, Osipova A.A., Smirnova M.P., Borodinova A.A., Volgushev M.A., Malyshev A.Y. Plasticity of response properties of mouse visual cortex neurons induced by optogenetic tetanization in vivo. Curr Issues Mol Biol. 2024. 46(4): 3294–3312.Stark E., Koos T., Buzsáki G. Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. J. Neurophysiol. 2012. 108(1): 349–363.Takeuchi T., Duszkiewicz A.J., Morris R.G.M. The synaptic plasticity and memory hypothesis: Encoding, storage and persistence. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2013. 369(1633): 20130288.Tsien J.Z. Linking Hebb’s coincidence-detection to memory formation. Curr. Opin. Neurobiol. 2000. 10(2): 266–273.Volgushev M., Voronin L.L., Chistiakova M., Singer W. Relations Between Long-term Synaptic Modifications and Paired-pulse Interactions in the Rat Neocortex. Eur. J. Neurosci. 1997. 9(8): 1656–1665.Wang H., Peca J., Matsuzaki M., Matsuzaki K., Noguchi J., Qiu L., Wang D., Zhang F., Boyden E., Deisseroth K., Kasai H., Hall W.C., Feng G., Augustine G.J. High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 2007. 104(19): 8143–8148.Wiesel T.N., Hubel D.H. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 1963. 26: 1003–1017.Yan Y., Rasch M.J., Chen M., Xiang X., Huang M., Wu S., Li W. Perceptual training continuously refines neuronal population codes in primary visual cortex. Nat. Neurosci. 2014. 17(10): 1380–1387.Yang T., Maunsell J.H.R. The effect of perceptual learning on neuronal responses in monkey visual area V4. J. Neurosci. 2004. 24(7): 1617–1626.Yao H., Dan Y. Stimulus Timing-Dependent Plasticity in Cortical Processing of Orientation. Neuron. 2001. 32(2): 315–323.Zenke F., Hennequin G., Gerstner W. Synaptic plasticity in neural networks needs homeostasis with a fast rate detector. PLoS Comput. Biol. 2013. 9 (11): e1003330.