{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,8]],"date-time":"2026-01-08T02:15:35Z","timestamp":1767838535437,"version":"3.49.0"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1010564","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,10,14]],"date-time":"2022-10-14T00:00:00Z","timestamp":1665705600000}}],"reference-count":83,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2022,10,4]],"date-time":"2022-10-04T00:00:00Z","timestamp":1664841600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100010661","name":"Horizon 2020 Framework Programme","doi-asserted-by":"publisher","award":["GA No.945539"],"award-info":[{"award-number":["GA No.945539"]}],"id":[{"id":"10.13039\/100010661","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Saccadic eye-movements play a crucial role in visuo-motor control by allowing rapid foveation onto new targets. However, the neural processes governing saccades adaptation are not fully understood. Saccades, due to the short-time of execution (20\u2013100 ms) and the absence of sensory information for online feedback control, must be controlled in a ballistic manner. Incomplete measurements of the movement trajectory, such as the visual endpoint error, are supposedly used to form internal predictions about the movement kinematics resulting in predictive control. In order to characterize the synaptic and neural circuit mechanisms underlying predictive saccadic control, we have reconstructed the saccadic system in a digital controller embedding a spiking neural network of the cerebellum with spike timing-dependent plasticity (STDP) rules driving parallel fiber\u2014Purkinje cell long-term potentiation and depression (LTP and LTD). This model implements a control policy based on a dual plasticity mechanism, resulting in the identification of the roles of LTP and LTD in regulating the overall quality of saccade kinematics: it turns out that LTD increases the accuracy by decreasing visual error and LTP increases the peak speed. The control policy also required cerebellar PCs to be divided into two subpopulations, characterized by burst or pause responses. To our knowledge, this is the first model that explains in mechanistic terms the visual error and peak speed regulation of ballistic eye movements in forward mode exploiting spike-timing to regulate firing in different populations of the neuronal network. This elementary model of saccades could be extended and applied to other more complex cases in which single jerks are concatenated to compose articulated and coordinated movements.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010564","type":"journal-article","created":{"date-parts":[[2022,10,4]],"date-time":"2022-10-04T17:33:41Z","timestamp":1664904821000},"page":"e1010564","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":11,"title":["Dual STDP processes at Purkinje cells contribute to distinct improvements in accuracy and speed of saccadic eye movements"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8294-6606","authenticated-orcid":true,"given":"Lorenzo","family":"Fruzzetti","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2634-7953","authenticated-orcid":true,"given":"Hari Teja","family":"Kalidindi","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0388-6321","authenticated-orcid":true,"given":"Alberto","family":"Antonietti","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0655-4189","authenticated-orcid":true,"given":"Cristiano","family":"Alessandro","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9407-8719","authenticated-orcid":true,"given":"Alice","family":"Geminiani","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8729-0391","authenticated-orcid":true,"given":"Claudia","family":"Casellato","sequence":"additional","affiliation":[]},{"given":"Egidio","family":"Falotico","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6007-7187","authenticated-orcid":true,"given":"Egidio","family":"D\u2019Angelo","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2022,10,4]]},"reference":[{"issue":"7\u20138","key":"pcbi.1010564.ref001","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1016\/S0893-6080(98)00066-5","article-title":"Multiple paired forward and inverse models for motor control.","volume":"11","author":"DM Wolpert","year":"1998","journal-title":"Neural Netw."},{"issue":"11","key":"pcbi.1010564.ref002","doi-asserted-by":"crossref","first-page":"1226","DOI":"10.1038\/nn963","article-title":"Optimal feedback control as a theory of motor coordination","volume":"5","author":"E Todorov","year":"2002","journal-title":"Nat Neurosci"},{"issue":"3","key":"pcbi.1010564.ref003","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1007\/s002210100876","article-title":"Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles","volume":"141","author":"R Lewis","year":"2001","journal-title":"Exp Brain Res"},{"issue":"7","key":"pcbi.1010564.ref004","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1038\/nrn1427","article-title":"Optimal feedback control and the neural basis of volitional motor control.","volume":"5","author":"SH Scott","year":"2004","journal-title":"Nat Rev Neurosci.Jul"},{"issue":"6088","key":"pcbi.1010564.ref005","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1038\/323533a0","article-title":"Learning representations by back-propagating errors","volume":"323","author":"DE Rumelhart","year":"1986","journal-title":"Nature"},{"issue":"11","key":"pcbi.1010564.ref006","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1016\/S1364-6613(00)01537-0","article-title":"Forward modeling allows feedback control for fast reaching movements.","volume":"4","author":"M Desmurget","year":"2000","journal-title":"Trends Cogn Sci."},{"issue":"48","key":"pcbi.1010564.ref007","doi-asserted-by":"crossref","first-page":"15213","DOI":"10.1523\/JNEUROSCI.4296-09.2009","article-title":"Subthreshold Activation of the Superior Colliculus Drives Saccade Motor Learning","volume":"29","author":"R Soetedjo","year":"2009","journal-title":"J Neurosci"},{"issue":"38","key":"pcbi.1010564.ref008","doi-asserted-by":"crossref","first-page":"E8987","DOI":"10.1073\/pnas.1806215115","article-title":"Elimination of the error signal in the superior colliculus impairs saccade motor learning","volume":"115","author":"Y Kojima","year":"2018","journal-title":"Proc Natl Acad Sci"},{"issue":"6","key":"pcbi.1010564.ref009","doi-asserted-by":"crossref","first-page":"2153","DOI":"10.1152\/jn.00781.2018","article-title":"How cerebellar motor learning keeps saccades accurate","volume":"121","author":"R Soetedjo","year":"2019","journal-title":"J Neurophysiol"},{"key":"pcbi.1010564.ref010","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1007\/978-1-4899-5379-7_5","volume-title":"Eye Movements and Vision [Internet]","author":"AL Yarbus","year":"1967"},{"key":"pcbi.1010564.ref011","volume-title":"The Control of Gaze. 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Shadmehr","year":"2020","journal-title":"J Neurophysiol"},{"key":"pcbi.1010564.ref046","first-page":"31","volume-title":"Chapter 2\u2014The Organization of Plasticity in the Cerebellar Cortex: From Synapses to Control.","author":"E. D\u2019Angelo","year":"2014"},{"issue":"3","key":"pcbi.1010564.ref047","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/0025-5564(75)90075-9","article-title":"The main sequence, a tool for studying human eye movements","volume":"24","author":"AT Bahill","year":"1975","journal-title":"Math Biosci"},{"issue":"3","key":"pcbi.1010564.ref048","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1113\/jphysiol.1967.sp008271","article-title":"Saccadic and smooth pursuit eye movements in the monkey","volume":"191","author":"AF Fuchs","year":"1967","journal-title":"J Physiol"},{"issue":"6","key":"pcbi.1010564.ref049","doi-asserted-by":"crossref","first-page":"2355","DOI":"10.1523\/JNEUROSCI.4064-13.2014","article-title":"Long-Term Potentiation at Cerebellar Parallel Fiber\u2013Purkinje Cell Synapses Requires Presynaptic and Postsynaptic Signaling Cascades","volume":"34","author":"DJ Wang","year":"2014","journal-title":"J Neurosci"},{"issue":"2","key":"pcbi.1010564.ref050","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.neuron.2006.09.032","article-title":"Synaptic Memories Upside Down: Bidirectional Plasticity at Cerebellar Parallel Fiber-Purkinje Cell Synapses","volume":"52","author":"H J\u00f6rntell","year":"2006","journal-title":"Neuron"},{"issue":"5","key":"pcbi.1010564.ref051","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1016\/S0896-6273(02)00713-4","article-title":"Reciprocal Bidirectional Plasticity of Parallel Fiber Receptive Fields in Cerebellar Purkinje Cells and Their Afferent Interneurons","volume":"34","author":"H J\u00f6rntell","year":"2002","journal-title":"Neuron"},{"issue":"5","key":"pcbi.1010564.ref052","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1038\/87419","article-title":"Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum","volume":"4","author":"C Hansel","year":"2001","journal-title":"Nat Neurosci"},{"issue":"9","key":"pcbi.1010564.ref053","doi-asserted-by":"crossref","first-page":"3363","DOI":"10.1111\/ejn.12700","article-title":"Cerebellar theta burst stimulation dissociates memory components in eyeblink classical conditioning","volume":"40","author":"J Monaco","year":"2014","journal-title":"Eur J Neurosci"},{"issue":"9","key":"pcbi.1010564.ref054","doi-asserted-by":"crossref","first-page":"1977","DOI":"10.1016\/j.celrep.2015.10.057","article-title":"Evolving Models of Pavlovian Conditioning: Cerebellar Cortical Dynamics in Awake Behaving Mice","volume":"13","author":"MM ten Brinke","year":"2015","journal-title":"Cell Rep"},{"issue":"5","key":"pcbi.1010564.ref055","doi-asserted-by":"crossref","first-page":"e1000085","DOI":"10.1371\/journal.pcbi.1000085","article-title":"Silent Synapses, LTP, and the Indirect Parallel-Fibre Pathway: Computational Consequences of Optimal Cerebellar Noise-Processing.","volume":"4","author":"J Porrill","year":"2008","journal-title":"PLOS Comput Biol."},{"issue":"9","key":"pcbi.1010564.ref056","doi-asserted-by":"crossref","first-page":"e3001400","DOI":"10.1371\/journal.pbio.3001400","article-title":"Cerebellar complex spikes multiplex complementary behavioral information","volume":"19","author":"A Markanday","year":"2021","journal-title":"PLOS Biol"},{"issue":"12","key":"pcbi.1010564.ref057","doi-asserted-by":"crossref","first-page":"1798","DOI":"10.1038\/nn.4167","article-title":"Climbing fibers encode a temporal-difference prediction error during cerebellar learning in mice","volume":"18","author":"S Ohmae","year":"2015","journal-title":"Nat Neurosci"},{"issue":"1","key":"pcbi.1010564.ref058","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S0165-0270(98)00063-6","article-title":"On the optimal control of behaviour: a stochastic perspective","volume":"83","author":"CM Harris","year":"1998","journal-title":"J Neurosci Methods"},{"issue":"1541","key":"pcbi.1010564.ref059","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1098\/rspb.2003.2658","article-title":"Recurrent cerebellar architecture solves the motor-error problem","volume":"271","author":"J Porrill","year":"2004","journal-title":"Proc R Soc Lond B Biol Sci"},{"issue":"3","key":"pcbi.1010564.ref060","doi-asserted-by":"crossref","first-page":"e33319","DOI":"10.1371\/journal.pone.0033319","article-title":"A Computational Mechanism for Unified Gain and Timing Control in the Cerebellum.","volume":"7","author":"T Yamazaki","year":"2012","journal-title":"PLOS ONE."},{"key":"pcbi.1010564.ref061","doi-asserted-by":"crossref","unstructured":"Franchi E, Falotico E, Zambrano D, Muscolo GG, Marazzato L, Dario P, et al. A comparison between two bio-inspired adaptive models of Vestibulo-Ocular Reflex (VOR) implemented on the iCub robot. In: 2010 10th IEEE-RAS International Conference on Humanoid Robots. 2010. p. 251\u20136.","DOI":"10.1109\/ICHR.2010.5686329"},{"key":"pcbi.1010564.ref062","doi-asserted-by":"crossref","first-page":"e31599","DOI":"10.7554\/eLife.31599","article-title":"Cerebellar learning using perturbations.","volume":"7","author":"G Bouvier","year":"2018","journal-title":"eLife"},{"issue":"1","key":"pcbi.1010564.ref063","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/S0896-6273(00)00004-0","article-title":"Gain Modulation: A Major Computational Principle of the Central Nervous System","volume":"27","author":"E Salinas","year":"2000","journal-title":"Neuron"},{"key":"pcbi.1010564.ref064","article-title":"Spontaneous recovery and the multiple timescales of human motor memory.","author":"SP Orozco","year":"2020","journal-title":"bioRxiv."},{"key":"pcbi.1010564.ref065","article-title":"Distributed cerebellar plasticity implements adaptable gain control in a manipulation task: a closed-loop robotic simulation.","author":"JA Garrido Alcazar","year":"2013","journal-title":"Front Neural Circuits [Internet]."},{"issue":"5","key":"pcbi.1010564.ref066","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1016\/j.neuron.2016.10.022","article-title":"Timing Rules for Synaptic Plasticity Matched to Behavioral Function","volume":"92","author":"A Suvrathan","year":"2016","journal-title":"Neuron"},{"key":"pcbi.1010564.ref067","first-page":"116","article-title":"Seeking a unified framework for cerebellar function and dysfunction: from circuit operations to cognition.","volume":"6","author":"E D\u2019Angelo","year":"2012","journal-title":"Front Neural Circuits"},{"issue":"9","key":"pcbi.1010564.ref068","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1167\/3.9.435","article-title":"A model for the adaptation of saccades by the cerebellum.","volume":"3","author":"M. Fujita","year":"2003","journal-title":"J Vis."},{"issue":"2","key":"pcbi.1010564.ref069","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1038\/s41583-020-00392-x","article-title":"Bidirectional learning in upbound and downbound microzones of the cerebellum.","volume":"22","author":"I C De Zeeuw","year":"2021","journal-title":"Nat Rev Neurosci."},{"issue":"8","key":"pcbi.1010564.ref070","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1016\/0042-6989(87)90210-0","article-title":"Planning sequences of saccades","volume":"27","author":"CM Zingale","year":"1987","journal-title":"Vision Res"},{"key":"pcbi.1010564.ref071","author":"R Rao","year":"1996","journal-title":"Learning Saccadic Eye Movements Using Multiscale Spatial Filters"},{"issue":"5","key":"pcbi.1010564.ref072","doi-asserted-by":"crossref","first-page":"e1002508","DOI":"10.1371\/journal.pcbi.1002508","article-title":"Optimal Control of Saccades by Spatial-Temporal Activity Patterns in the Monkey Superior 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Smith","year":"2006","journal-title":"PLOS Biol"},{"issue":"6","key":"pcbi.1010564.ref076","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1007\/s00422-008-0219-z","article-title":"Linear ensemble-coding in midbrain superior colliculus specifies the saccade kinematics.","volume":"98","author":"AJ van Opstal","year":"2008","journal-title":"Biol Cybern."},{"key":"pcbi.1010564.ref077","article-title":"PyNEST: a convenient interface to the NEST simulator.","volume":"2","author":"J Eppler","year":"2009","journal-title":"Front Neuroinformatics [Internet]."},{"issue":"2","key":"pcbi.1010564.ref078","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s10827-006-7949-5","article-title":"Parallel network simulations with NEURON","volume":"21","author":"M Migliore","year":"2006","journal-title":"J Comput Neurosci"},{"issue":"1\u20132","key":"pcbi.1010564.ref079","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.biosystems.2008.05.008","article-title":"A real-time spiking cerebellum model for learning robot control.","volume":"94","author":"RR Carrillo","year":"2008","journal-title":"Biosystems."},{"issue":"8","key":"pcbi.1010564.ref080","doi-asserted-by":"crossref","first-page":"1321","DOI":"10.1109\/TNN.2011.2156809","article-title":"Cerebellar Input Configuration Toward Object Model Abstraction in Manipulation Tasks","volume":"22","author":"NR Luque","year":"2011","journal-title":"IEEE Trans Neural Netw"},{"key":"pcbi.1010564.ref081","doi-asserted-by":"crossref","first-page":"e4862157","DOI":"10.1155\/2019\/4862157","article-title":"Control of a Humanoid NAO Robot by an Adaptive Bioinspired Cerebellar Module in 3D Motion Tasks.","volume":"2019","author":"A Antonietti","year":"2019","journal-title":"Comput Intell Neurosci."},{"issue":"11","key":"pcbi.1010564.ref082","doi-asserted-by":"crossref","first-page":"4744","DOI":"10.1109\/TCYB.2019.2899246","article-title":"VOR Adaptation on a Humanoid iCub Robot Using a Spiking Cerebellar 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