• Soichi Nagao.
• Laboratory for Integrative Brain Function, Nozomi Hospital, Komuro 3170, Ina, Kitaadachi-gun, Saitama 362-0806, Japan; Laboratory for Memory Neuroscience, Tokyo Metropolotan Institute for Gerontology, Sakae-cho, Itabashi-ku, Tokyo 173-0015, Japan. Electronic address: nagao-so@umin.ac.jp.
• Neuroscience. 2021 May 10; 462: 191-204.

AbstractMasao Ito proposed a cerebellar learning hypothesis with Marr and Albus in the early 1970s. He suggested that cerebellar flocculus (FL) Purkinje cells (PCs), which directly inhibit the vestibular nuclear neurons driving extraocular muscle motor neurons, adaptively control the horizontal vestibulo-ocular reflex (HVOR) through the modification of mossy and parallel fiber-mediated vestibular responsiveness by visual climbing fiber (CF) inputs. Later, it was suggested that the same FL PCs adaptively control the horizontal optokinetic response (HOKR) in the same manner through the modification of optokinetic responsiveness in rodents and rabbits. In 1982, Ito and his colleagues discovered the plasticity of long-term depression (LTD) at parallel fiber (PF)-PC synapses after conjunctive stimulation of mossy or parallel fibers with CFs. Long-term potentiation (LTP) at PF-PC synapses by weak PF stimulation alone was found later. Many lines of experimental evidence have supported their hypothesis using various experimental methods and materials for the past 50 years by many research groups. Although several controversial findings were presented regarding their hypothesis, the reasons underlying many of them were clarified. Today, their hypothesis is considered as a fundamental mechanism of cerebellar learning. Furthermore, it was found that the memory of adaptation is transferred from the FL to vestibular nuclei for consolidation by repetition of adaptation through the plasticity of vestibular nuclear neurons. In this article, after overviewing their cerebellar learning hypothesis, I discuss possible roles of LTD and LTP in gain-up and gain-down HVOR/HOKR adaptations and refer to the expansion of their hypothesis to cognitive functions.Copyright © 2020 IBRO. Published by Elsevier Ltd. All rights reserved.

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