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Article ; Online: Developmental synapse remodeling in the cerebellum and visual thalamus.

Kano, Masanobu / Watanabe, Takaki

2019 Volume 8

Abstract: Functional neural circuits of mature animals are shaped during postnatal development by eliminating early-formed redundant synapses and strengthening of necessary connections. In the nervous system of newborn animals, redundant synapses are only ... ...

Abstract	Functional neural circuits of mature animals are shaped during postnatal development by eliminating early-formed redundant synapses and strengthening of necessary connections. In the nervous system of newborn animals, redundant synapses are only transient features of the circuit. During subsequent postnatal development, some synapses are strengthened whereas other redundant connections are weakened and eventually eliminated. In this review, we introduce recent studies on the mechanisms of developmental remodeling of climbing fiber-to-Purkinje cell synapses in the cerebellum and synapses from the retina to neurons in the dorsal lateral geniculate nucleus of the visual thalamus (retinogeniculate synapses). These are the two representative models of developmental synapse remodeling in the brain and they share basic principles, including dependency on neural activity. However, recent studies have disclosed that, in several respects, the two models use different molecules and strategies to establish mature synaptic connectivity. We describe similarities and differences between the two models and discuss remaining issues to be tackled in the future in order to understand the general schemes of developmental synapse remodeling.
MeSH term(s)	Animals ; Animals, Newborn ; Cerebellum/growth & development ; Neuronal Plasticity ; Neurons ; Purkinje Cells ; Retina ; Synapses/physiology ; Thalamus/growth & development
Language	English
Publishing date	2019-07-25
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2699932-8
ISSN	2046-1402 ; 2046-1402
ISSN (online)	2046-1402
ISSN	2046-1402
DOI	10.12688/f1000research.18903.1
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Article ; Online: Combining electrophysiology and optogenetics for functional screening of pyramidal neurons in the mouse prefrontal cortex.

Nagahama, Kenichiro / Fujino, Shuhei / Watanabe, Takaki / Uesaka, Naofumi / Kano, Masanobu

STAR protocols

2021 Volume 2, Issue 2, Page(s) 100469

Abstract: Here, we present a comprehensive protocol to analyze the roles of disease-related genes in synaptic transmission. We have developed a pipeline of electrophysiological techniques and combined these with optogenetics in the medial prefrontal cortex of mice. ...

Abstract	Here, we present a comprehensive protocol to analyze the roles of disease-related genes in synaptic transmission. We have developed a pipeline of electrophysiological techniques and combined these with optogenetics in the medial prefrontal cortex of mice. This methodology provides a cost-effective, faster, and easier screening approach to elucidate functional aspects of single genes in several regions in the mouse brain such as a specific layer of the mPFC. For complete details on the use and execution of this protocol, please refer to Nagahama et al. (2020) and Sacai et al. (2020).
MeSH term(s)	Animals ; Mice ; Neural Pathways/metabolism ; Optogenetics ; Prefrontal Cortex/metabolism ; Pyramidal Cells/metabolism ; Synaptic Transmission
Language	English
Publishing date	2021-04-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2666-1667
ISSN (online)	2666-1667
DOI	10.1016/j.xpro.2021.100469
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Article: Type-1 metabotropic glutamate receptor signaling in cerebellar Purkinje cells in health and disease.

Kano, Masanobu / Watanabe, Takaki

F1000Research

2017 Volume 6, Page(s) 416

Abstract: The cerebellum is a brain structure involved in coordination, control, and learning of movements, as well as certain aspects of cognitive function. Purkinje cells are the sole output neurons from the cerebellar cortex and therefore play crucial roles in ... ...

Abstract	The cerebellum is a brain structure involved in coordination, control, and learning of movements, as well as certain aspects of cognitive function. Purkinje cells are the sole output neurons from the cerebellar cortex and therefore play crucial roles in the overall function of the cerebellum. The type-1 metabotropic glutamate receptor (mGluR1) is a key "hub" molecule that is critically involved in the regulation of synaptic wiring, excitability, synaptic response, and synaptic plasticity of Purkinje cells. In this review, we aim to highlight how mGluR1 controls these events in Purkinje cells. We also describe emerging evidence that altered mGluR1 signaling in Purkinje cells underlies cerebellar dysfunctions in several clinically relevant mouse models of human ataxias.
Language	English
Publishing date	2017
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2699932-8
ISSN	2046-1402
ISSN	2046-1402
DOI	10.12688/f1000research.10485.1
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Article: PTPδ is a presynaptic organizer for the formation and maintenance of climbing fiber to Purkinje cell synapses in the developing cerebellum.

Okuno, Yuto / Sakoori, Kazuto / Matsuyama, Kyoko / Yamasaki, Miwako / Watanabe, Masahiko / Hashimoto, Kouichi / Watanabe, Takaki / Kano, Masanobu

Frontiers in molecular neuroscience

2023 Volume 16, Page(s) 1206245

Abstract: Functionally mature neural circuits are shaped during postnatal development by eliminating redundant synapses formed during the perinatal period. In the cerebellum of neonatal rodents, each Purkinje cell (PC) receives synaptic inputs from multiple (more ... ...

Abstract	Functionally mature neural circuits are shaped during postnatal development by eliminating redundant synapses formed during the perinatal period. In the cerebellum of neonatal rodents, each Purkinje cell (PC) receives synaptic inputs from multiple (more than 4) climbing fibers (CFs). During the first 3 postnatal weeks, synaptic inputs from a single CF become markedly larger and those from the other CFs are eliminated in each PC, leading to mono-innervation of each PC by a strong CF in adulthood. While molecules involved in the strengthening and elimination of CF synapses during postnatal development are being elucidated, much less is known about the molecular mechanisms underlying CF synapse formation during the early postnatal period. Here, we show experimental evidence that suggests that a synapse organizer, PTPδ, is required for early postnatal CF synapse formation and the subsequent establishment of CF to PC synaptic wiring. We showed that PTPδ was localized at CF-PC synapses from postnatal day 0 (P0) irrespective of the expression of Aldolase C (Aldoc), a major marker of PC that distinguishes the cerebellar compartments. We found that the extension of a single strong CF along PC dendrites (CF translocation) was impaired in global PTPδ knockout (KO) mice from P12 to P29-31 predominantly in PCs that did not express Aldoc [Aldoc (-) PCs]. We also demonstrated via morphological and electrophysiological analyses that the number of CFs innervating individual PCs in PTPδ KO mice were fewer than in wild-type (WT) mice from P3 to P13 with a significant decrease in the strength of CF synaptic inputs in cerebellar anterior lobules where most PCs are Aldoc (-). Furthermore, CF-specific PTPδ-knockdown (KD) caused a reduction in the number of CFs innervating PCs with decreased CF synaptic inputs at P10-13 in anterior lobules. We found a mild impairment of motor performance in adult PTPδ KO mice. These results indicate that PTPδ acts as a presynaptic organizer for CF-PC formation and is required for normal CF-PC synaptic transmission, CF translocation, and presumably CF synapse maintenance predominantly in Aldoc (-) PCs. Furthermore, this study suggests that the impaired CF-PC synapse formation and development by the lack of PTPδ causes mild impairment of motor performance.
Language	English
Publishing date	2023-06-22
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452967-9
ISSN	1662-5099
ISSN	1662-5099
DOI	10.3389/fnmol.2023.1206245
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Article: [Postnatal Development of Cerebellar Neural Circuits].

Watanabe, Takaki / Suzuki, Honoka / Kano, Masanobu

Brain and nerve = Shinkei kenkyu no shinpo

2019 Volume 71, Issue 12, Page(s) 1373–1383

Abstract: Prof. Masao Ito contributed greatly to the elucidation of the structure and function of cerebellar neuronal circuits. He formulated a cerebellar motor learning theory and an internal model hypothesis and pursued how complex cerebellar functions resulted ... ...

Abstract	Prof. Masao Ito contributed greatly to the elucidation of the structure and function of cerebellar neuronal circuits. He formulated a cerebellar motor learning theory and an internal model hypothesis and pursued how complex cerebellar functions resulted from the operation of neural circuits. In this article, we first provide a brief overview of the major cell types and the synaptic organization of cerebellar neural circuits. Then we introduce how mature cerebellar neural circuits are shaped through synapse formation and pruning during postnatal development. We also refer to the maturation of inhibitory neurons and glial cells during postnatal development.
MeSH term(s)	Cerebellum/growth & development ; Humans ; Neuroglia/physiology ; Neurons/physiology ; Synapses
Language	Japanese
Publishing date	2019-11-28
Publishing country	Japan
Document type	Journal Article ; Review
ZDB-ID	390389-8
ISSN	1344-8129 ; 1881-6096 ; 0006-8969
ISSN (online)	1344-8129
ISSN	1881-6096 ; 0006-8969
DOI	10.11477/mf.1416201457
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Article: [Mechanisms of synapse pruning in the developing cerebellum].

Watanabe, Takaki / Uesaka, Naofumi / Kano, Masanobu

Seikagaku. The Journal of Japanese Biochemical Society

2018 Volume 88, Issue 5, Page(s) 621–629

MeSH term(s)	Animals ; Cell Differentiation ; Cerebellum/cytology ; Cerebellum/growth & development ; Cerebellum/metabolism ; Humans ; Neurogenesis ; Signal Transduction ; Synapses/metabolism
Language	Japanese
Publishing date	2018-04-06
Publishing country	Japan
Document type	Journal Article ; Review
ZDB-ID	282319-6
ISSN	0037-1017
ISSN	0037-1017
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Article ; Online: Multiple Phases of Climbing Fiber Synapse Elimination in the Developing Cerebellum.

Kano, Masanobu / Watanabe, Takaki / Uesaka, Naofumi / Watanabe, Masahiko

Cerebellum (London, England)

2018 Volume 17, Issue 6, Page(s) 722–734

Abstract: Functional neural circuits in the mature animals are shaped during postnatal development by elimination of unnecessary synapses and strengthening of necessary ones among redundant synaptic connections formed transiently around birth. In the cerebellum of ...

Abstract	Functional neural circuits in the mature animals are shaped during postnatal development by elimination of unnecessary synapses and strengthening of necessary ones among redundant synaptic connections formed transiently around birth. In the cerebellum of neonatal rodents, excitatory synapses are formed on the somata of Purkinje cells (PCs) by climbing fibers (CFs) that originate from neurons in the contralateral inferior olive. Each PC receives inputs from multiple (~ five) CFs that have about equal synaptic strengths. Subsequently, a single CF selectively becomes stronger relative to the other CFs during the first postnatal week. Then, from around postnatal day 9 (P9), only the strongest CF ("winner" CF) extends its synaptic territory along PC dendrites. In contrast, synapses of the weaker CFs ("loser" CFs) remain on the soma and the most proximal portion of the dendrite together with somatic synapses of the "winner" CF. These perisomatic CF synapses are eliminated progressively during the second and the third postnatal weeks. From P6 to P11, the elimination proceeds independently of the formation of the synapses on PC dendrites by parallel fibers (PFs). From P12 and thereafter, the elimination requires normal PF-PC synapse formation and is presumably dependent on the PF synaptic inputs. Most PCs become mono-innervated by single strong CFs on their dendrites in the third postnatal week. In this review article, we will describe how adult-type CF mono-innervation of PC is established through these multiple phases of postnatal cerebellar development and make an overview of molecular/cellular mechanisms underlying them.
MeSH term(s)	Animals ; Cerebellum/cytology ; Cerebellum/growth & development ; Cerebellum/physiology ; Neural Pathways/cytology ; Neural Pathways/growth & development ; Neural Pathways/physiology ; Neurons/cytology ; Neurons/physiology ; Olivary Nucleus/cytology ; Olivary Nucleus/growth & development ; Olivary Nucleus/physiology ; Synapses/physiology
Language	English
Publishing date	2018-08-18
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	2112586-7
ISSN	1473-4230 ; 1473-4222
ISSN (online)	1473-4230
ISSN	1473-4222
DOI	10.1007/s12311-018-0964-z
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Article ; Online: mGluR5 Is Substitutable for mGluR1 in Cerebellar Purkinje Cells for Motor Coordination, Developmental Synapse Elimination, and Motor Learning.

Harbers, Maria / Nakao, Harumi / Watanabe, Takaki / Matsuyama, Kyoko / Tohyama, Shoichi / Nakao, Kazuki / Kishimoto, Yasushi / Kano, Masanobu / Aiba, Atsu

Cells

2022 Volume 11, Issue 13

Abstract: Group I metabotropic glutamate receptors (mGluRs) include mGluR1 and mGluR5, which are coupled to the Gq family of heterotrimeric G-proteins and readily activated by their selective agonist 3,5-dihydroxyphenilglycine (DHPG). mGluR1 and mGluR5 exhibit ... ...

Abstract	Group I metabotropic glutamate receptors (mGluRs) include mGluR1 and mGluR5, which are coupled to the Gq family of heterotrimeric G-proteins and readily activated by their selective agonist 3,5-dihydroxyphenilglycine (DHPG). mGluR1 and mGluR5 exhibit nearly complementary distributions spatially or temporally in the central nervous system (CNS). In adult cerebellar Purkinje cells (PCs), mGluR1 is a dominant group I mGluR and mGluR5 is undetectable. mGluR1 expression increases substantially during the first three weeks of postnatal development and remains high throughout adulthood. On the other hand, mGluR5 expression is observed during the first two postnatal weeks and then decreases. However, functional differences between mGluR1 and mGluR5 in the CNS remains to be elucidated. To address this issue, we generated "mGluR5-rescue" mice in which mGluR5 is specifically expressed in PCs in global mGluR1-knockout (KO) mice. mGluR5-rescue mice exhibited apparently normal motor coordination, developmental elimination of redundant climbing fiber (CF)-PC synapses, and delay eyeblink conditioning, which were severely impaired in mGluR1-KO mice. We concluded that mGluR5 is functionally comparable with mGluR1 in cerebellar PCs.
MeSH term(s)	Animals ; Mice ; Mice, Knockout ; Purkinje Cells/physiology ; Receptor, Metabotropic Glutamate 5/metabolism ; Receptors, Metabotropic Glutamate ; Synapses/metabolism
Chemical Substances	Grm5 protein, mouse ; Receptor, Metabotropic Glutamate 5 ; Receptors, Metabotropic Glutamate ; metabotropic glutamate receptor type 1
Language	English
Publishing date	2022-06-23
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells11132004
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Article ; Online: Phospholipase C β3 is Required for Climbing Fiber Synapse Elimination in Aldolase C-positive Compartments of the Developing Mouse Cerebellum.

Rai, Yurie / Watanabe, Takaki / Matsuyama, Kyoko / Sakimura, Kenji / Uesaka, Naofumi / Kano, Masanobu

Neuroscience

2020 Volume 462, Page(s) 36–43

Abstract: In the cerebellum of neonatal mice, multiple climbing fibers (CFs) form excitatory synapses on each Purkinje cell (PC). Only one CF is strengthened in each PC from postnatal day 3 (P3) to P7, whereas the other weaker CFs are eliminated progressively from ...

Abstract	In the cerebellum of neonatal mice, multiple climbing fibers (CFs) form excitatory synapses on each Purkinje cell (PC). Only one CF is strengthened in each PC from postnatal day 3 (P3) to P7, whereas the other weaker CFs are eliminated progressively from ∼P7 to ∼P11 (early phase of CF elimination) and from ∼P12 to ∼P17 (late phase of CF elimination). Type 1 metabotropic glutamate receptor (mGluR1) triggers a canonical pathway in PCs for the late phase of CF elimination. Among downstream signaling molecules of mGluR1, phospholipase C β3 (PLCβ3) and β4 (PLCβ4) are expressed complementarily in PCs of aldolase C (Aldoc)-positive (+) and Aldoc-negative (-) cerebellar compartments, respectively. PLCβ4 is reported to mediate the late phase of CF elimination in the anterior half of the cerebellar vermis which corresponds to the Aldoc (-) region. However, roles of PLCβ3 and Aldoc in CF synapse elimination are unknown. Here, we investigated CF innervation of PCs in Aldoc-tdTomato knock-in mice that underwent lentivirus-mediated knockdown (KD) of PLCβ3 in PCs during postnatal development. By recording CF-mediated excitatory postsynaptic currents from PCs and immunostaining CF synaptic terminals, we found that significantly higher percentage of PCs with PLCβ3-KD remained multiply innervated by CFs in Aldoc (+) compartments after P12, which was accompanied by impaired elimination of somatic CF synapses and reduced dendritic CF translocation. In contrast, deletion of Aldoc had no effect on CF synapse elimination. These results suggest that PLCβ3 is required for the late phase of CF elimination in Aldoc (+) PCs.
MeSH term(s)	Animals ; Cerebellum ; Fructose-Bisphosphate Aldolase ; Mice ; Nerve Fibers ; Phospholipase C beta ; Purkinje Cells ; Synapses
Chemical Substances	Phospholipase C beta (EC 3.1.4.11) ; Plcb3 protein, mouse (EC 3.1.4.11) ; Fructose-Bisphosphate Aldolase (EC 4.1.2.13)
Language	English
Publishing date	2020-04-29
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	196739-3
ISSN	1873-7544 ; 0306-4522
ISSN (online)	1873-7544
ISSN	0306-4522
DOI	10.1016/j.neuroscience.2020.04.035
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Article ; Online: Coordinated Expression of Two Types of Low-Threshold K

Watanabe, Takaki / Shimazaki, Takashi / Oda, Yoichi

eNeuro

2017 Volume 4, Issue 5

Abstract: Expression of different ion channels permits homologously-generated neurons to acquire different types of excitability and thus code various kinds of input information. Mauthner (M) series neurons in the teleost hindbrain consist of M cells and their ... ...

Abstract	Expression of different ion channels permits homologously-generated neurons to acquire different types of excitability and thus code various kinds of input information. Mauthner (M) series neurons in the teleost hindbrain consist of M cells and their morphological homologs, which are repeated in adjacent segments and share auditory inputs. When excited, M cells generate a single spike at the onset of abrupt stimuli, while their homologs encode input intensity with firing frequency. Our previous study in zebrafish showed that immature M cells burst phasically at 2 d postfertilization (dpf) and acquire single spiking at 4 dpf by specific expression of auxiliary Kvβ2 subunits in M cells in association with common expression of Kv1.1 channels in the M series. Here, we further reveal the ionic mechanisms underlying this functional differentiation. Pharmacological blocking of Kv7/KCNQ in addition to Kv1 altered mature M cells to fire tonically, similar to the homologs. In contrast, blocking either channel alone caused M cells to burst phasically. M cells at 2 dpf fired tonically after blocking Kv7.
Language	English
Publishing date	2017-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	2800598-3
ISSN	2373-2822 ; 2373-2822
ISSN (online)	2373-2822
ISSN	2373-2822
DOI	10.1523/ENEURO.0249-17.2017
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