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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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Remodeling of Purkinje dendrites in the third postnatal week.A: Confocal and graphic images of dendrites in a P35 Purkinje cell. Some branches extrude from the main sagittal plane and overpass other branches (magenta circles). Scale bar: 10 µm. B–F: Quantitative analyses of dendrite development in Purkinje cells in lobules IX and X. The number (B) and total length (C) of branches per cell rapidly increase over the first 18 postnatal days. Both the number and length significantly decrease between P18 and P22, and further increase into adulthood. D: Overpassing branches per cell peak at P18, sharply decrease by P22 and plateau thereafter. E: The mean length of each dendritic branch decreases between P7 and P9, constantly increases until P35 and then slightly decreased by P50. F: The total sagittal-sectional area of the molecular layer covered by the dendrite increases until P35 with a plateau between P18 and P22. Purkinje cells per data point in C–G: P7, P14–P50, n = 14; P9, n = 20. Error bars indicate s.e.m. G: Histogram showing the developmental change in percentages of multiplanar Purkinje cells. The percentage of multiplanar Purkinje cells peaks at P18 in both early and late maturing lobules (lobules IX, X and lobules III–VIII, respectively). The number of cells analyzed is indicated in parentheses.
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pone-0020108-g002: Remodeling of Purkinje dendrites in the third postnatal week.A: Confocal and graphic images of dendrites in a P35 Purkinje cell. Some branches extrude from the main sagittal plane and overpass other branches (magenta circles). Scale bar: 10 µm. B–F: Quantitative analyses of dendrite development in Purkinje cells in lobules IX and X. The number (B) and total length (C) of branches per cell rapidly increase over the first 18 postnatal days. Both the number and length significantly decrease between P18 and P22, and further increase into adulthood. D: Overpassing branches per cell peak at P18, sharply decrease by P22 and plateau thereafter. E: The mean length of each dendritic branch decreases between P7 and P9, constantly increases until P35 and then slightly decreased by P50. F: The total sagittal-sectional area of the molecular layer covered by the dendrite increases until P35 with a plateau between P18 and P22. Purkinje cells per data point in C–G: P7, P14–P50, n = 14; P9, n = 20. Error bars indicate s.e.m. G: Histogram showing the developmental change in percentages of multiplanar Purkinje cells. The percentage of multiplanar Purkinje cells peaks at P18 in both early and late maturing lobules (lobules IX, X and lobules III–VIII, respectively). The number of cells analyzed is indicated in parentheses.

Mentions: A higher magnified view revealed that most branches of mature Purkinje dendrites at P35 extended in a single sagittal plane with minimal contacts or overlap (Figure 2A). In contrast, branches extending in differential sagittal planes passed over other branches without physical contact. These overpassing dendrites appeared to overlap with other branches when the three-dimensional image stacks were viewed sagittally (magenta circles in Figure 2A).


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)

Remodeling of Purkinje dendrites in the third postnatal week.A: Confocal and graphic images of dendrites in a P35 Purkinje cell. Some branches extrude from the main sagittal plane and overpass other branches (magenta circles). Scale bar: 10 µm. B–F: Quantitative analyses of dendrite development in Purkinje cells in lobules IX and X. The number (B) and total length (C) of branches per cell rapidly increase over the first 18 postnatal days. Both the number and length significantly decrease between P18 and P22, and further increase into adulthood. D: Overpassing branches per cell peak at P18, sharply decrease by P22 and plateau thereafter. E: The mean length of each dendritic branch decreases between P7 and P9, constantly increases until P35 and then slightly decreased by P50. F: The total sagittal-sectional area of the molecular layer covered by the dendrite increases until P35 with a plateau between P18 and P22. Purkinje cells per data point in C–G: P7, P14–P50, n = 14; P9, n = 20. Error bars indicate s.e.m. G: Histogram showing the developmental change in percentages of multiplanar Purkinje cells. The percentage of multiplanar Purkinje cells peaks at P18 in both early and late maturing lobules (lobules IX, X and lobules III–VIII, respectively). The number of cells analyzed is indicated in parentheses.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3105010&req=5

pone-0020108-g002: Remodeling of Purkinje dendrites in the third postnatal week.A: Confocal and graphic images of dendrites in a P35 Purkinje cell. Some branches extrude from the main sagittal plane and overpass other branches (magenta circles). Scale bar: 10 µm. B–F: Quantitative analyses of dendrite development in Purkinje cells in lobules IX and X. The number (B) and total length (C) of branches per cell rapidly increase over the first 18 postnatal days. Both the number and length significantly decrease between P18 and P22, and further increase into adulthood. D: Overpassing branches per cell peak at P18, sharply decrease by P22 and plateau thereafter. E: The mean length of each dendritic branch decreases between P7 and P9, constantly increases until P35 and then slightly decreased by P50. F: The total sagittal-sectional area of the molecular layer covered by the dendrite increases until P35 with a plateau between P18 and P22. Purkinje cells per data point in C–G: P7, P14–P50, n = 14; P9, n = 20. Error bars indicate s.e.m. G: Histogram showing the developmental change in percentages of multiplanar Purkinje cells. The percentage of multiplanar Purkinje cells peaks at P18 in both early and late maturing lobules (lobules IX, X and lobules III–VIII, respectively). The number of cells analyzed is indicated in parentheses.
Mentions: A higher magnified view revealed that most branches of mature Purkinje dendrites at P35 extended in a single sagittal plane with minimal contacts or overlap (Figure 2A). In contrast, branches extending in differential sagittal planes passed over other branches without physical contact. These overpassing dendrites appeared to overlap with other branches when the three-dimensional image stacks were viewed sagittally (magenta circles in Figure 2A).

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