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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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Purkinje cells are consistently multiplanar in the sulcus.A: The percentage of multiplanar Purkinje cells in distinct foliar subdivisions. The number of cells analyzed is indicated in parentheses. Remodeling from multiplanar to monoplanar dendrites is retarded in Purkinje cells in the sulcus. B: Confocal (left) and graphic (right) images of CFs and a multiplanar Purkinje cell in the sulcus. CFs in the sulcal region are radially arranged so that minor CFs tend to access the lateral side of the Purkinje cell. C: The Purkinje cell shown in B dissociated in three different sagittal planes. Scale bars: 20 µm.
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pone-0020108-g004: Purkinje cells are consistently multiplanar in the sulcus.A: The percentage of multiplanar Purkinje cells in distinct foliar subdivisions. The number of cells analyzed is indicated in parentheses. Remodeling from multiplanar to monoplanar dendrites is retarded in Purkinje cells in the sulcus. B: Confocal (left) and graphic (right) images of CFs and a multiplanar Purkinje cell in the sulcus. CFs in the sulcal region are radially arranged so that minor CFs tend to access the lateral side of the Purkinje cell. C: The Purkinje cell shown in B dissociated in three different sagittal planes. Scale bars: 20 µm.

Mentions: In studying Purkinje cell morphology, we noticed that cells in the sulcal fundus often exhibited multiplanar arrangement even in adult stages. We thus compared dendritic configurations in three distinct subdivisions of the cerebellar folia (gyrus, bank and sulcus). Purkinje cells were arranged radially so that their dendrites densely overlapped with each other due to the concave shape of the molecular layer in the sulcus. Purkinje cells in the sulcus consistently exhibited multiplanar structures at higher percentage than in the gyrus and bank, and the difference was statistically significant (Figure 4A; P25–35; 48.8%, n = 41, sulcus vs. 23.9%, n = 201, bank; p<0.05; χ2 test). The multiplanar Purkinje cells in the sulcus were apposed to multiple CFs extended from the overlapping dendrites of other Purkinje cells (Figure 4B,C).


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)

Purkinje cells are consistently multiplanar in the sulcus.A: The percentage of multiplanar Purkinje cells in distinct foliar subdivisions. The number of cells analyzed is indicated in parentheses. Remodeling from multiplanar to monoplanar dendrites is retarded in Purkinje cells in the sulcus. B: Confocal (left) and graphic (right) images of CFs and a multiplanar Purkinje cell in the sulcus. CFs in the sulcal region are radially arranged so that minor CFs tend to access the lateral side of the Purkinje cell. C: The Purkinje cell shown in B dissociated in three different sagittal planes. Scale bars: 20 µm.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020108-g004: Purkinje cells are consistently multiplanar in the sulcus.A: The percentage of multiplanar Purkinje cells in distinct foliar subdivisions. The number of cells analyzed is indicated in parentheses. Remodeling from multiplanar to monoplanar dendrites is retarded in Purkinje cells in the sulcus. B: Confocal (left) and graphic (right) images of CFs and a multiplanar Purkinje cell in the sulcus. CFs in the sulcal region are radially arranged so that minor CFs tend to access the lateral side of the Purkinje cell. C: The Purkinje cell shown in B dissociated in three different sagittal planes. Scale bars: 20 µm.
Mentions: In studying Purkinje cell morphology, we noticed that cells in the sulcal fundus often exhibited multiplanar arrangement even in adult stages. We thus compared dendritic configurations in three distinct subdivisions of the cerebellar folia (gyrus, bank and sulcus). Purkinje cells were arranged radially so that their dendrites densely overlapped with each other due to the concave shape of the molecular layer in the sulcus. Purkinje cells in the sulcus consistently exhibited multiplanar structures at higher percentage than in the gyrus and bank, and the difference was statistically significant (Figure 4A; P25–35; 48.8%, n = 41, sulcus vs. 23.9%, n = 201, bank; p<0.05; χ2 test). The multiplanar Purkinje cells in the sulcus were apposed to multiple CFs extended from the overlapping dendrites of other Purkinje cells (Figure 4B,C).

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