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Remodeling of monoplanar Purkinje cell dendrites during cerebellar circuit formation.

Kaneko M, Yamaguchi K, Eiraku M, Sato M, Takata N, Kiyohara Y, Mishina M, Hirase H, Hashikawa T, Kengaku M - PLoS ONE (2011)

Bottom Line: Dendrites then became confined to a single plane in the fourth postnatal week.The dendrite remodeling was also impaired by pharmacological disruption of normal afferent activity during the second or third postnatal week.Our results suggest that the monoplanar arborization of Purkinje cells is coupled with functional development of the cerebellar circuitry.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Neural Cell Polarity, RIKEN Brain Science Institute, Wako, Saitama, Japan.

ABSTRACT
Dendrite arborization patterns are critical determinants of neuronal connectivity and integration. Planar and highly branched dendrites of the cerebellar Purkinje cell receive specific topographical projections from two major afferent pathways; a single climbing fiber axon from the inferior olive that extend along Purkinje dendrites, and parallel fiber axons of granule cells that contact vertically to the plane of dendrites. It has been believed that murine Purkinje cell dendrites extend in a single parasagittal plane in the molecular layer after the cell polarity is determined during the early postnatal development. By three-dimensional confocal analysis of growing Purkinje cells, we observed that mouse Purkinje cells underwent dynamic dendritic remodeling during circuit maturation in the third postnatal week. After dendrites were polarized and flattened in the early second postnatal week, dendritic arbors gradually expanded in multiple sagittal planes in the molecular layer by intensive growth and branching by the third postnatal week. Dendrites then became confined to a single plane in the fourth postnatal week. Multiplanar Purkinje cells in the third week were often associated by ectopic climbing fibers innervating nearby Purkinje cells in distinct sagittal planes. The mature monoplanar arborization was disrupted in mutant mice with abnormal Purkinje cell connectivity and motor discoordination. The dendrite remodeling was also impaired by pharmacological disruption of normal afferent activity during the second or third postnatal week. Our results suggest that the monoplanar arborization of Purkinje cells is coupled with functional development of the cerebellar circuitry.

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Impaired remodeling of Purkinje dendrites in GluRδ2- or GLAST-deficient mice.A: Cellular morphology of P30 Purkinje cells in wildtype, GluRδ2-deficient (δ2−/−) and GLAST-deficient (GLAST−/−) mice from sagittal (left panels) and coronal (right panels) views. The coronal views show irregular, multiplanar arrangement of dendrites in the GluRδ2−/− and GLAST−/− mice in contrast to the monoplanar appearance in the wildtype mouse. Dendrites in minor sagittal planes are pseudocolored in graphic images. B: High power sagittal views of dendrites in wildtype and mutant mice in respective boxed regions in A. Dendrites significantly overpass one another in sagittal views in GluRδ2−/− and GLAST−/− mice. C: Quantitative comparison of dendrite morphology of GluRδ2−/− and GLAST −/− Purkinje cells with respective wildtype littermates. Cells in the bank region of lobules IX and X were analyzed. n = 10 cells for each data point, mean±s.e.m., Student's t test, *p<0.01. Scale bars: 20 µm.
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pone-0020108-g005: Impaired remodeling of Purkinje dendrites in GluRδ2- or GLAST-deficient mice.A: Cellular morphology of P30 Purkinje cells in wildtype, GluRδ2-deficient (δ2−/−) and GLAST-deficient (GLAST−/−) mice from sagittal (left panels) and coronal (right panels) views. The coronal views show irregular, multiplanar arrangement of dendrites in the GluRδ2−/− and GLAST−/− mice in contrast to the monoplanar appearance in the wildtype mouse. Dendrites in minor sagittal planes are pseudocolored in graphic images. B: High power sagittal views of dendrites in wildtype and mutant mice in respective boxed regions in A. Dendrites significantly overpass one another in sagittal views in GluRδ2−/− and GLAST−/− mice. C: Quantitative comparison of dendrite morphology of GluRδ2−/− and GLAST −/− Purkinje cells with respective wildtype littermates. Cells in the bank region of lobules IX and X were analyzed. n = 10 cells for each data point, mean±s.e.m., Student's t test, *p<0.01. Scale bars: 20 µm.

Mentions: We next explored the conditions under which dendrite remodeling is impaired. We analyzed the dendritic configuration of Purkinje cells in GluRδ2-deficient mice to assess the correlation with normal Purkinje cell connectivity. Glutamate Receptor δ2 subunit is a member of the ionotropic glutamate receptor that is highly enriched in Purkinje cells. GluRδ2-deficient mice exhibit significant reduction in PF-Purkinje cell synapses, expansion of CF territory and ectopic CF innervation. Further, long-term depression of PF-Purkinje cell synapses, motor learning and motor coordination are impaired in GluRδ2-deficient mice [13], [38], [39]. In contrast to previous observation that Purkinje dendrite morphology was unaffected in GluRδ2-deficient mice, the monoplanar arborization was significantly disrupted in mutants as compared to wildtype littermates (Figure 5A, C; multiplanar cells; 22.3%, n = 112, P30 wildtype vs. 47.3%, n = 112, P30 GluRδ2-deficient mutant, p<0.01; χ2 test). From a sagittal view, dendritic branches significantly overpassed one another in GluRδ2-deficient mice (Figure 5B). Quantitative assessments revealed that GluRδ2 deficiency induced a marked increase in branch overpasses, and a slight decrease in the area occupied by the dendrite in a sagittal plane (Figure 5C). Other aspects of dendrite morphology including the number, total length of branches, and the mean branch length were not affected by GluRδ2 deficiency.


Remodeling of monoplanar Purkinje cell dendrites during cerebellar circuit formation.

Kaneko M, Yamaguchi K, Eiraku M, Sato M, Takata N, Kiyohara Y, Mishina M, Hirase H, Hashikawa T, Kengaku M - PLoS ONE (2011)

Impaired remodeling of Purkinje dendrites in GluRδ2- or GLAST-deficient mice.A: Cellular morphology of P30 Purkinje cells in wildtype, GluRδ2-deficient (δ2−/−) and GLAST-deficient (GLAST−/−) mice from sagittal (left panels) and coronal (right panels) views. The coronal views show irregular, multiplanar arrangement of dendrites in the GluRδ2−/− and GLAST−/− mice in contrast to the monoplanar appearance in the wildtype mouse. Dendrites in minor sagittal planes are pseudocolored in graphic images. B: High power sagittal views of dendrites in wildtype and mutant mice in respective boxed regions in A. Dendrites significantly overpass one another in sagittal views in GluRδ2−/− and GLAST−/− mice. C: Quantitative comparison of dendrite morphology of GluRδ2−/− and GLAST −/− Purkinje cells with respective wildtype littermates. Cells in the bank region of lobules IX and X were analyzed. n = 10 cells for each data point, mean±s.e.m., Student's t test, *p<0.01. Scale bars: 20 µm.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3105010&req=5

pone-0020108-g005: Impaired remodeling of Purkinje dendrites in GluRδ2- or GLAST-deficient mice.A: Cellular morphology of P30 Purkinje cells in wildtype, GluRδ2-deficient (δ2−/−) and GLAST-deficient (GLAST−/−) mice from sagittal (left panels) and coronal (right panels) views. The coronal views show irregular, multiplanar arrangement of dendrites in the GluRδ2−/− and GLAST−/− mice in contrast to the monoplanar appearance in the wildtype mouse. Dendrites in minor sagittal planes are pseudocolored in graphic images. B: High power sagittal views of dendrites in wildtype and mutant mice in respective boxed regions in A. Dendrites significantly overpass one another in sagittal views in GluRδ2−/− and GLAST−/− mice. C: Quantitative comparison of dendrite morphology of GluRδ2−/− and GLAST −/− Purkinje cells with respective wildtype littermates. Cells in the bank region of lobules IX and X were analyzed. n = 10 cells for each data point, mean±s.e.m., Student's t test, *p<0.01. Scale bars: 20 µm.
Mentions: We next explored the conditions under which dendrite remodeling is impaired. We analyzed the dendritic configuration of Purkinje cells in GluRδ2-deficient mice to assess the correlation with normal Purkinje cell connectivity. Glutamate Receptor δ2 subunit is a member of the ionotropic glutamate receptor that is highly enriched in Purkinje cells. GluRδ2-deficient mice exhibit significant reduction in PF-Purkinje cell synapses, expansion of CF territory and ectopic CF innervation. Further, long-term depression of PF-Purkinje cell synapses, motor learning and motor coordination are impaired in GluRδ2-deficient mice [13], [38], [39]. In contrast to previous observation that Purkinje dendrite morphology was unaffected in GluRδ2-deficient mice, the monoplanar arborization was significantly disrupted in mutants as compared to wildtype littermates (Figure 5A, C; multiplanar cells; 22.3%, n = 112, P30 wildtype vs. 47.3%, n = 112, P30 GluRδ2-deficient mutant, p<0.01; χ2 test). From a sagittal view, dendritic branches significantly overpassed one another in GluRδ2-deficient mice (Figure 5B). Quantitative assessments revealed that GluRδ2 deficiency induced a marked increase in branch overpasses, and a slight decrease in the area occupied by the dendrite in a sagittal plane (Figure 5C). Other aspects of dendrite morphology including the number, total length of branches, and the mean branch length were not affected by GluRδ2 deficiency.

Bottom Line: Dendrites then became confined to a single plane in the fourth postnatal week.The dendrite remodeling was also impaired by pharmacological disruption of normal afferent activity during the second or third postnatal week.Our results suggest that the monoplanar arborization of Purkinje cells is coupled with functional development of the cerebellar circuitry.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Neural Cell Polarity, RIKEN Brain Science Institute, Wako, Saitama, Japan.

ABSTRACT
Dendrite arborization patterns are critical determinants of neuronal connectivity and integration. Planar and highly branched dendrites of the cerebellar Purkinje cell receive specific topographical projections from two major afferent pathways; a single climbing fiber axon from the inferior olive that extend along Purkinje dendrites, and parallel fiber axons of granule cells that contact vertically to the plane of dendrites. It has been believed that murine Purkinje cell dendrites extend in a single parasagittal plane in the molecular layer after the cell polarity is determined during the early postnatal development. By three-dimensional confocal analysis of growing Purkinje cells, we observed that mouse Purkinje cells underwent dynamic dendritic remodeling during circuit maturation in the third postnatal week. After dendrites were polarized and flattened in the early second postnatal week, dendritic arbors gradually expanded in multiple sagittal planes in the molecular layer by intensive growth and branching by the third postnatal week. Dendrites then became confined to a single plane in the fourth postnatal week. Multiplanar Purkinje cells in the third week were often associated by ectopic climbing fibers innervating nearby Purkinje cells in distinct sagittal planes. The mature monoplanar arborization was disrupted in mutant mice with abnormal Purkinje cell connectivity and motor discoordination. The dendrite remodeling was also impaired by pharmacological disruption of normal afferent activity during the second or third postnatal week. Our results suggest that the monoplanar arborization of Purkinje cells is coupled with functional development of the cerebellar circuitry.

Show MeSH
Related in: MedlinePlus