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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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Confocal analysis of dendrite arborization in developing Purkinje cells.A: Sagittal (left) and coronal (right) views of developing Purkinje cells labeled with adeno-associated virus (AAV)-derived GFP. Three-dimensional images were compiled from 20–50 z-serial sections taken at 1 µm intervals. Dendritic processes at P7 orient randomly in the molecular layer. At P9 and thereafter, Purkinje cells bear a single to a few primary stem dendrites which extend branches along the sagittal axis of the molecular layer. B: Confocal and graphic images of typical Purkinje cells at P18. Sagittal (left panels) and coronal (right panels) views are shown. Some dendrites extrude from the sagittal plane filled by main arbors, and further branch in distinct parallel sagittal planes (pseudocolored in yellow and blue in graphic images; see also Video S1). C: The P22 Purkinje cell arborizes dendrites in a single sagittal plane (see also Video S2). Scale bars: 20 µm.
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pone-0020108-g001: Confocal analysis of dendrite arborization in developing Purkinje cells.A: Sagittal (left) and coronal (right) views of developing Purkinje cells labeled with adeno-associated virus (AAV)-derived GFP. Three-dimensional images were compiled from 20–50 z-serial sections taken at 1 µm intervals. Dendritic processes at P7 orient randomly in the molecular layer. At P9 and thereafter, Purkinje cells bear a single to a few primary stem dendrites which extend branches along the sagittal axis of the molecular layer. B: Confocal and graphic images of typical Purkinje cells at P18. Sagittal (left panels) and coronal (right panels) views are shown. Some dendrites extrude from the sagittal plane filled by main arbors, and further branch in distinct parallel sagittal planes (pseudocolored in yellow and blue in graphic images; see also Video S1). C: The P22 Purkinje cell arborizes dendrites in a single sagittal plane (see also Video S2). Scale bars: 20 µm.

Mentions: It has been shown that Purkinje cell somata extend multiple dendrites in random orientations during the first postnatal week of murine development. A single primary dendrite is determined during the second postnatal week, which rapidly extends and branches in a single parasagittal (translobular) plane [15], [30], [31], [32]. Consistent with previous observations, Purkinje dendrites underwent a dynamic remodeling around the first to second postnatal weeks (Figure 1A, S2). At P7, many Purkinje cells exhibited a multipolar morphology with multiple small processes emanating from the cell body (Figure S2 and Video S1). These perisomatic processes had few branches and randomly oriented in all three dimensions of the molecular layer. In the second postnatal week (P9), most Purkinje cells became flat with a single primary stem dendrite that aligned along the sagittal axis (Figure S2 and Video S2). This remodeling has been observed around P12 in rats [31], consistent with previous findings that the cerebellar cortex matures earlier in the mouse than in the rat [33]. From the third postnatal week, the primary dendrite rapidly extended and branched along the sagittal (translobular) axis of the cerebellar cortex until the beginning of the sixth postnatal week (from P14 to P35). There was little apparent change in the size and complexity of dendrites between P35 and P50.


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)

Confocal analysis of dendrite arborization in developing Purkinje cells.A: Sagittal (left) and coronal (right) views of developing Purkinje cells labeled with adeno-associated virus (AAV)-derived GFP. Three-dimensional images were compiled from 20–50 z-serial sections taken at 1 µm intervals. Dendritic processes at P7 orient randomly in the molecular layer. At P9 and thereafter, Purkinje cells bear a single to a few primary stem dendrites which extend branches along the sagittal axis of the molecular layer. B: Confocal and graphic images of typical Purkinje cells at P18. Sagittal (left panels) and coronal (right panels) views are shown. Some dendrites extrude from the sagittal plane filled by main arbors, and further branch in distinct parallel sagittal planes (pseudocolored in yellow and blue in graphic images; see also Video S1). C: The P22 Purkinje cell arborizes dendrites in a single sagittal plane (see also Video S2). Scale bars: 20 µm.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020108-g001: Confocal analysis of dendrite arborization in developing Purkinje cells.A: Sagittal (left) and coronal (right) views of developing Purkinje cells labeled with adeno-associated virus (AAV)-derived GFP. Three-dimensional images were compiled from 20–50 z-serial sections taken at 1 µm intervals. Dendritic processes at P7 orient randomly in the molecular layer. At P9 and thereafter, Purkinje cells bear a single to a few primary stem dendrites which extend branches along the sagittal axis of the molecular layer. B: Confocal and graphic images of typical Purkinje cells at P18. Sagittal (left panels) and coronal (right panels) views are shown. Some dendrites extrude from the sagittal plane filled by main arbors, and further branch in distinct parallel sagittal planes (pseudocolored in yellow and blue in graphic images; see also Video S1). C: The P22 Purkinje cell arborizes dendrites in a single sagittal plane (see also Video S2). Scale bars: 20 µm.
Mentions: It has been shown that Purkinje cell somata extend multiple dendrites in random orientations during the first postnatal week of murine development. A single primary dendrite is determined during the second postnatal week, which rapidly extends and branches in a single parasagittal (translobular) plane [15], [30], [31], [32]. Consistent with previous observations, Purkinje dendrites underwent a dynamic remodeling around the first to second postnatal weeks (Figure 1A, S2). At P7, many Purkinje cells exhibited a multipolar morphology with multiple small processes emanating from the cell body (Figure S2 and Video S1). These perisomatic processes had few branches and randomly oriented in all three dimensions of the molecular layer. In the second postnatal week (P9), most Purkinje cells became flat with a single primary stem dendrite that aligned along the sagittal axis (Figure S2 and Video S2). This remodeling has been observed around P12 in rats [31], consistent with previous findings that the cerebellar cortex matures earlier in the mouse than in the rat [33]. From the third postnatal week, the primary dendrite rapidly extended and branched along the sagittal (translobular) axis of the cerebellar cortex until the beginning of the sixth postnatal week (from P14 to P35). There was little apparent change in the size and complexity of dendrites between P35 and P50.

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