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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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Disrupted remodeling of Purkinje dendrites in harmaline-treated mice.Cellular morphology of P30 Purkinje cells in mice treated with saline (A) and harmaline (B) at P9–P14. Dendrites become irregular and multiplanar by harmaline treatment compared to the control littermate. Dendrites in minor sagittal planes are pseudocolored in graphic images. C: High power sagittal views of dendrites in respective boxed regions in A and B. Dendrites significantly overpass one another in harmaline-treated mice. D: Quantitative comparison of dendrite morphology in mice treated with saline or harmaline during P9–P14 or P15–P20. Overpassing branches are significantly increased by harmaline treatment in either period. Cells in the bank region of lobules IV and V were analyzed. n = 10 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-g006: Disrupted remodeling of Purkinje dendrites in harmaline-treated mice.Cellular morphology of P30 Purkinje cells in mice treated with saline (A) and harmaline (B) at P9–P14. Dendrites become irregular and multiplanar by harmaline treatment compared to the control littermate. Dendrites in minor sagittal planes are pseudocolored in graphic images. C: High power sagittal views of dendrites in respective boxed regions in A and B. Dendrites significantly overpass one another in harmaline-treated mice. D: Quantitative comparison of dendrite morphology in mice treated with saline or harmaline during P9–P14 or P15–P20. Overpassing branches are significantly increased by harmaline treatment in either period. Cells in the bank region of lobules IV and V were analyzed. n = 10 for each data point, mean±s.e.m, Student's t test, *p<0.01. Scale bars: 20 µm.

Mentions: We next examined the effect of abnormal afferent activity on Purkinje cell morphology. Systemic administration of harmaline induces a synchronous and enhanced firing of inferior olive neurons in mice [42], [43], [44]. It has also been shown that chronic application during the second postnatal week induces sustained multiple CF innervation in rats until adult ages [45]. We administered harmaline (30 mg/kg) by daily intraperitoneal injections for 6 days during the second (P9–P14) or the third (P15–P20) postnatal week, and assayed Purkinje cell morphology at P30. Harmaline treatment caused no gross abnormalities in mouse cerebellar cortex as previously reported [46]. We found that chronic application of harmaline during the second or the third postnatal week induced association of ectopic CFs in distal dendrites at P30 in mice (Figure S6). A majority of Purkinje cells in animals treated with harmaline either in the second or third postnatal week displayed multiplanar morphology at P30, while those in untreated control animals had mostly completed monoplanar rearrangement at this stage (Figure 6A, B; multiplanar cells; 27.1%, n = 96, control vs. 54.6%, n = 108, harmaline P9–P14, p<0.01; 25.3%, n = 75, control vs. 49.4%, n = 89, harmaline P15–P20, p<0.05; χ2 test). Overall dendritic growth was unaffected by harmaline treatment except for the striking increase in overpassing branches in a sagittal view (Figure 6C, D). These results strongly suggest that normal afferent inputs are critical for dendritic remodeling of Purkinje cells from multiplanar to monoplanar configurations.


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)

Disrupted remodeling of Purkinje dendrites in harmaline-treated mice.Cellular morphology of P30 Purkinje cells in mice treated with saline (A) and harmaline (B) at P9–P14. Dendrites become irregular and multiplanar by harmaline treatment compared to the control littermate. Dendrites in minor sagittal planes are pseudocolored in graphic images. C: High power sagittal views of dendrites in respective boxed regions in A and B. Dendrites significantly overpass one another in harmaline-treated mice. D: Quantitative comparison of dendrite morphology in mice treated with saline or harmaline during P9–P14 or P15–P20. Overpassing branches are significantly increased by harmaline treatment in either period. Cells in the bank region of lobules IV and V were analyzed. n = 10 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-g006: Disrupted remodeling of Purkinje dendrites in harmaline-treated mice.Cellular morphology of P30 Purkinje cells in mice treated with saline (A) and harmaline (B) at P9–P14. Dendrites become irregular and multiplanar by harmaline treatment compared to the control littermate. Dendrites in minor sagittal planes are pseudocolored in graphic images. C: High power sagittal views of dendrites in respective boxed regions in A and B. Dendrites significantly overpass one another in harmaline-treated mice. D: Quantitative comparison of dendrite morphology in mice treated with saline or harmaline during P9–P14 or P15–P20. Overpassing branches are significantly increased by harmaline treatment in either period. Cells in the bank region of lobules IV and V were analyzed. n = 10 for each data point, mean±s.e.m, Student's t test, *p<0.01. Scale bars: 20 µm.
Mentions: We next examined the effect of abnormal afferent activity on Purkinje cell morphology. Systemic administration of harmaline induces a synchronous and enhanced firing of inferior olive neurons in mice [42], [43], [44]. It has also been shown that chronic application during the second postnatal week induces sustained multiple CF innervation in rats until adult ages [45]. We administered harmaline (30 mg/kg) by daily intraperitoneal injections for 6 days during the second (P9–P14) or the third (P15–P20) postnatal week, and assayed Purkinje cell morphology at P30. Harmaline treatment caused no gross abnormalities in mouse cerebellar cortex as previously reported [46]. We found that chronic application of harmaline during the second or the third postnatal week induced association of ectopic CFs in distal dendrites at P30 in mice (Figure S6). A majority of Purkinje cells in animals treated with harmaline either in the second or third postnatal week displayed multiplanar morphology at P30, while those in untreated control animals had mostly completed monoplanar rearrangement at this stage (Figure 6A, B; multiplanar cells; 27.1%, n = 96, control vs. 54.6%, n = 108, harmaline P9–P14, p<0.01; 25.3%, n = 75, control vs. 49.4%, n = 89, harmaline P15–P20, p<0.05; χ2 test). Overall dendritic growth was unaffected by harmaline treatment except for the striking increase in overpassing branches in a sagittal view (Figure 6C, D). These results strongly suggest that normal afferent inputs are critical for dendritic remodeling of Purkinje cells from multiplanar to monoplanar configurations.

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