Multiple innervation of cerebellar Purkinje cells by climbing fibres in staggerer mutant mouse

Crépel, F.; Delhaye‐Bouchaud, Nicole; Guastavino, J.-M.; SAMPAIO, I. S.

doi:10.1038/283483a0

Cited by 132 publications

(61 citation statements)

References 18 publications

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“…We found large-scale pruning of the branches of these axons over the course of vocal learning, unlike axon arbors that have been described in other developing systems (Crepel et al, 1976(Crepel et al, , 1980Lichtman, 1977;Smolen and Raisman, 1979;Changeux, 1980, 1981;Johnson and Purves, 1981;Shatz, 1984, 1986;Rubin, 1985;Young and Rubel, 1986;Callaway and Katz, 1991;Agmon et al, 1993;Antonini and Stryker, 1993;Catalano et al, 1996;Gan and Lichtman, 1998). Additionally, the dramatic changes in overall volume of the DLM terminal field within lMAN could be explained by changes in spatial extent and degree of overlap between individual DLM axon arbors.…”

Section: Abstract: Axons; Songbirds; Vocal Learning; Topographic; Rementioning

confidence: 72%

Development of Individual Axon Arbors in a Thalamocortical Circuit Necessary for Song Learning in Zebra Finches

Iyengar

Bottjer

2002

J. Neurosci.

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Individual axon arbors within developing neural circuits are remodeled during restricted sensitive periods, leading to the emergence of precise patterns of connectivity and specialized adaptive behaviors. In male zebra finches, the circuit connecting the medial dorsolateral nucleus of the thalamus (DLM) and its cortical target, the lateral magnocellular nucleus of the anterior neostriatum (lMAN), is crucial for the acquisition of a normal vocal pattern during the sensitive period for song learning. The shell subregion of lMAN as well as the entire terminal field of DLM axons within lMAN undergo a striking increase in overall volume during early stages of vocal learning followed by an equally substantial decrease by adulthood, by which time birds have acquired stable song patterns. Because the total number of DLM neurons remains stable throughout this period, the dramatic changes within the overall DLM3lMAN circuit are presumably attributable to dynamic rearrangements at the level of individual DLM axon arbors over the course of vocal learning.To study such rearrangements directly, we reconstructed individual DLM axon arbors in three dimensions at different stages during vocal learning. Unlike axon arbors in other model systems, in which the number of branches increases during development, DLM arbors are unusual in that they have the greatest number of branches at the onset of vocal learning and undergo large-scale retraction during the sensitive period for song learning. Decreases in the degree of overlap between DLM arbors apparently contribute to the increased overall volume of the DLM3lMAN circuit during vocal learning. These developmental changes in DLM axon arbors occur at the height of the sensitive period for vocal learning, and hence may represent either a morphological correlate of song learning or a necessary prerequisite for acquisition of song. Key words: axons; songbirds; vocal learning; topographic; remodeling; terminalsHighly ordered patterns of connectivity within different neural circuits and the specialized behaviors that they subserve emerge during restricted sensitive periods of development. The initial formation of connections between groups of presynaptic and postsynaptic neurons is characterized by considerable specificity; early patterns of axonal connectivity appear to be genetically predetermined and do not depend on sensory experience (Catalano et al., 1991;Crair et al., 1998;Crowley and Katz, 1999). Adult patterns of connectivity emerge at the culmination of sensitive periods during a later activity-dependent phase when sensory experience is thought to refine these neural circuits at the level of individual axon arbors and synapses (Goodman and

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Section: Abstract: Axons; Songbirds; Vocal Learning; Topographic; Rementioning

confidence: 72%

Development of Individual Axon Arbors in a Thalamocortical Circuit Necessary for Song Learning in Zebra Finches

Iyengar

Bottjer

2002

J. Neurosci.

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“…These mice include reeler (Mariani et al 1977), weaver Puro & Woodward 1977) and staggerer (Crepel et al 1980;Mariani & Changeux 1980). The multiple innervation also persists in the animals whose migrating granule cells are destroyed by X-ray irradiation (Woodward et al 1974;Crepel et al 1981) or by infection of a mink enteritis virus (Benoit et al 1987).…”

Section: Synapse Eliminationmentioning

confidence: 99%

Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination

Kano

Hashimoto

Tabata

2008

Phil. Trans. R. Soc. B

106

113

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The cerebellum is a brain structure involved in the coordination, control and learning of movements, and elucidation of its function is an important issue. Japanese scholars have made seminal contributions in this field of neuroscience. Electrophysiological studies of the cerebellum have a long history in Japan since the pioneering works by Ito and Sasaki. Elucidation of the basic circuit diagram of the cerebellum in the 1960s was followed by the construction of cerebellar network theories and finding of their neural correlates in the 1970s. A theoretically predicted synaptic plasticity, long-term depression (LTD) at parallel fibre to Purkinje cell synapse, was demonstrated experimentally in 1982 by Ito and co-workers. Since then, Japanese neuroscientists from various disciplines participated in this field and have made major contributions to elucidate molecular mechanisms underlying LTD. An important pathway for LTD induction is type-1 metabotropic glutamate receptor (mGluR1) and its downstream signal transduction in Purkinje cells. Sugiyama and co-workers demonstrated the presence of mGluRs and Nakanishi and his pupils identified the molecular structures and functions of the mGluR family. Moreover, the authors contributed to the discovery and elucidation of several novel functions of mGluR1 in cerebellar Purkinje cells. mGluR1 turned out to be crucial for the release of endocannabinoid from Purkinje cells and the resultant retrograde suppression of transmitter release. It was also found that mGluR1 and its downstream signal transduction in Purkinje cells are indispensable for the elimination of redundant synapses during post-natal cerebellar development. This article overviews the seminal works by Japanese neuroscientists, focusing on mGluR1 signalling in cerebellar Purkinje cells.

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“…Simultaneously, the pericellular nests are displaced progressively toward "peridendritic" innervation (Chedotal and Sotelo, 1992). Analyses of classical agranular animal models elucidate that PF-PC synaptogenesis is a prerequisite for developmental elimination of surplus CFs (Woodward et al, 1974;Crepel et al, 1980;Mariani, 1982;Bravin et al, 1995;Sugihara et al, 2000). Studies using gene knock-out mice have extended our knowledge that glutamate receptors play important roles in the excitatory synaptic wiring to PCs (Kano et al, 1995(Kano et al, , 1998Kashiwabuchi et al, 1995;Kurihara et al, 1997;Offermanns et al, 1997;Ichise et al, 2000;Hashimoto et al, 2001;Ichikawa et al, 2002).…”

Section: Introductionmentioning

confidence: 98%

P/Q-Type Ca²⁺Channel α1A Regulates Synaptic Competition on Developing Cerebellar Purkinje Cells

Miyazaki

Hashimoto²,

Shin³

et al. 2004

J. Neurosci.

135

126

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Synapse formation depends critically on the competition among inputs of multiple sources to individual neurons. Cerebellar Purkinje cells have highly organized synaptic wiring from two distinct sources of excitatory afferents. Single climbing fibers innervate proximal dendrites of Purkinje cells, whereas numerous parallel fibers converge on their distal dendrites. Here, we demonstrate that the P/Q-type Ca 2ϩ channel ␣1A, a major Ca 2ϩ channel subtype in Purkinje cells, is crucial for this organized synapse formation. In the ␣1A knock-out mouse, many ectopic spines were protruded from proximal dendrites and somata of Purkinje cells. Innervation territory of parallel fibers was expanded proximally to innervate the ectopic spines, whereas that of climbing fibers was regressed to the basal portion of proximal dendrites and somata. Furthermore, multiple climbing fibers consisting of a strong climbing fiber and one or a few weaker climbing fibers, persisted in the majority of Purkinje cells and were cowired to the same somata, proximal dendrites, or both. Therefore, the lack of ␣1A results in the persistence of parallel fibers and surplus climbing fibers, which should normally be expelled from the compartment innervated by the main climbing fiber. These results suggest that a P/Q-type Ca 2ϩ channel ␣1A fuels heterosynaptic competition between climbing fibers and parallel fibers and also fuels homosynaptic competition among multiple climbing fibers. This molecular function facilitates the distal extension of climbing fiber innervation along the dendritic tree of the Purkinje cell and also establishes climbing fiber monoinnervation of individual Purkinje cells.

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Multiple innervation of cerebellar Purkinje cells by climbing fibres in staggerer mutant mouse

Cited by 132 publications

References 18 publications

Development of Individual Axon Arbors in a Thalamocortical Circuit Necessary for Song Learning in Zebra Finches

Development of Individual Axon Arbors in a Thalamocortical Circuit Necessary for Song Learning in Zebra Finches

Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination

P/Q-Type Ca²⁺Channel α1A Regulates Synaptic Competition on Developing Cerebellar Purkinje Cells

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Multiple innervation of cerebellar Purkinje cells by climbing fibres in staggerer mutant mouse

Cited by 132 publications

References 18 publications

Development of Individual Axon Arbors in a Thalamocortical Circuit Necessary for Song Learning in Zebra Finches

Development of Individual Axon Arbors in a Thalamocortical Circuit Necessary for Song Learning in Zebra Finches

Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination

P/Q-Type Ca2+Channel α1A Regulates Synaptic Competition on Developing Cerebellar Purkinje Cells

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P/Q-Type Ca²⁺Channel α1A Regulates Synaptic Competition on Developing Cerebellar Purkinje Cells