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Dendritic planarity of Purkinje cells is independent of Reelin signaling.

Kim J, Park TJ, Kwon N, Lee D, Kim S, Kohmura Y, Ishikawa T, Kim KT, Curran T, Je JH - Brain Struct Funct (2014)

Bottom Line: Purkinje cells that failed to migrate completely exhibited conical dendrites with abnormal 3-D arborization and reduced dendritic complexity.In contrast, Purkinje cells that migrated successfully displayed planar dendritic and spine morphologies similar to normal cells, despite reduced dendritic complexity.While Reelin signaling is important for the migration process, it does not make a direct major contribution to dendrite formation.

View Article: PubMed Central - PubMed

Affiliation: X-ray Imaging Center, School of Interdisciplinary Bioscience and Bioengineering, Pohang University of Science and Technology (POSTECH), Pohang, 790-784, South Korea.

ABSTRACT
The dendritic planarity of Purkinje cells is critical for cerebellar circuit formation. In the absence of Crk and CrkL, the Reelin pathway does not function resulting in partial Purkinje cell migration and defective dendritogenesis. However, the relationships among Purkinje cell migration, dendritic development and Reelin signaling have not been clearly delineated. Here, we use synchrotron X-ray microscopy to obtain 3-D images of Golgi-stained Purkinje cell dendrites. Purkinje cells that failed to migrate completely exhibited conical dendrites with abnormal 3-D arborization and reduced dendritic complexity. Furthermore, their spines were fewer in number with a distorted morphology. In contrast, Purkinje cells that migrated successfully displayed planar dendritic and spine morphologies similar to normal cells, despite reduced dendritic complexity. These results indicate that, during cerebellar formation, Purkinje cells migrate into an environment that supports development of dendritic planarity and spine formation. While Reelin signaling is important for the migration process, it does not make a direct major contribution to dendrite formation.

No MeSH data available.


Related in: MedlinePlus

Quantitative characterization of planarity of PC dendrites. a–c 3-D tomographic volume-rendered image of a normal, a migrated and a non-migrated Crk/CrkL knockout PC (Movie S6–8). Here, y–z defines the sagittal plane, x–z, the coronal plane, and x–y, the transverse plane. d–f Projections on the x–y plane of the dendritic branch (green dots) and the end (blue dots) points from the images of panels a–c, respectively. The soma is marked by a red circle at the origin. F is the formula for ‘flattening’ ratio, F = (a − b)/a (a is the length of the semi-major axis in the projections; b is its semi-minor axis). g Angular distribution in the x–y plane of the dendritic branch and the end points for 5 normal (black), 5 migrated mutant (blue), and 10 non-migrated mutant (red) PC. The plot shows the percentage of the points found in each 10-degree angular interval. The error bars correspond to the SEM. h Flattening ratio of PC projections with the distance from the cerebellar surface (DCS) for 5 normal, 5 migrated mutant (the light blue region), and 10 non-migrated mutant (the pink region: n = 3 for DCS = 200–400 μm; n = 3 for DCS = 400–600 μm; n = 4 for DCS = 600–800 μm) PC. The error bars correspond to the SEM
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Fig3: Quantitative characterization of planarity of PC dendrites. a–c 3-D tomographic volume-rendered image of a normal, a migrated and a non-migrated Crk/CrkL knockout PC (Movie S6–8). Here, y–z defines the sagittal plane, x–z, the coronal plane, and x–y, the transverse plane. d–f Projections on the x–y plane of the dendritic branch (green dots) and the end (blue dots) points from the images of panels a–c, respectively. The soma is marked by a red circle at the origin. F is the formula for ‘flattening’ ratio, F = (a − b)/a (a is the length of the semi-major axis in the projections; b is its semi-minor axis). g Angular distribution in the x–y plane of the dendritic branch and the end points for 5 normal (black), 5 migrated mutant (blue), and 10 non-migrated mutant (red) PC. The plot shows the percentage of the points found in each 10-degree angular interval. The error bars correspond to the SEM. h Flattening ratio of PC projections with the distance from the cerebellar surface (DCS) for 5 normal, 5 migrated mutant (the light blue region), and 10 non-migrated mutant (the pink region: n = 3 for DCS = 200–400 μm; n = 3 for DCS = 400–600 μm; n = 4 for DCS = 600–800 μm) PC. The error bars correspond to the SEM

Mentions: The branching patterns of neurons are critical determinants of connectivity and integration (Greg Stuart and Hausser 1999; Mainen and Sejnowski 1996; Javier and Kreitzer 2012). To quantify the branching patterns of PC dendrites in normal and Crk/CrkL mutant mice, we examined high-resolution microtomographic images. Figure 3a–c shows 3-D volume-rendered images of PC from normal mice, as well as those representing migrated and non-migrated PC from Crk/CrkL mutant mice. The elaborate planar dendritic structure of PC was clearly detected in normal cerebellum using this method (Fig. 3a; Movie S6). Interestingly, migrated PC in Crk/CrkL mutant mice also displayed this characteristic planar feature (Fig. 3b; Movie S7); however, in non-migrated PC, dendrites were distributed in a conical array lacking any planar orientation (Fig. 3c; Movie S8). The 3-D volume-rendered images in Fig. 3a–c were used to calculate branch points and dendrite end points, which were projected as green and blue dots, respectively in Fig. 3d–f. In the case of normal PC and migrated PC in Crk/CrkL mutant mice, projections aligned along the y-axis, indicating a sagittal planar dendritic structure. In contrast, in non-migrated PC, no planar features were evident and dendrites were distributed randomly in the x–y plane. To quantitate the degree of planarity of the normal, we applied a formula for assessing the ‘flattening’ ratio, F = (a − b)/a (a is the length of the semi-major axis in the projections; b is its semi-minor axis). The flattening ratio was high in migrated mutant PC (F = 0.81), similar to that in normal PC (F = 0.90), but it was significantly reduced in non-migrated PC (F = 0.20).Fig. 3


Dendritic planarity of Purkinje cells is independent of Reelin signaling.

Kim J, Park TJ, Kwon N, Lee D, Kim S, Kohmura Y, Ishikawa T, Kim KT, Curran T, Je JH - Brain Struct Funct (2014)

Quantitative characterization of planarity of PC dendrites. a–c 3-D tomographic volume-rendered image of a normal, a migrated and a non-migrated Crk/CrkL knockout PC (Movie S6–8). Here, y–z defines the sagittal plane, x–z, the coronal plane, and x–y, the transverse plane. d–f Projections on the x–y plane of the dendritic branch (green dots) and the end (blue dots) points from the images of panels a–c, respectively. The soma is marked by a red circle at the origin. F is the formula for ‘flattening’ ratio, F = (a − b)/a (a is the length of the semi-major axis in the projections; b is its semi-minor axis). g Angular distribution in the x–y plane of the dendritic branch and the end points for 5 normal (black), 5 migrated mutant (blue), and 10 non-migrated mutant (red) PC. The plot shows the percentage of the points found in each 10-degree angular interval. The error bars correspond to the SEM. h Flattening ratio of PC projections with the distance from the cerebellar surface (DCS) for 5 normal, 5 migrated mutant (the light blue region), and 10 non-migrated mutant (the pink region: n = 3 for DCS = 200–400 μm; n = 3 for DCS = 400–600 μm; n = 4 for DCS = 600–800 μm) PC. The error bars correspond to the SEM
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Fig3: Quantitative characterization of planarity of PC dendrites. a–c 3-D tomographic volume-rendered image of a normal, a migrated and a non-migrated Crk/CrkL knockout PC (Movie S6–8). Here, y–z defines the sagittal plane, x–z, the coronal plane, and x–y, the transverse plane. d–f Projections on the x–y plane of the dendritic branch (green dots) and the end (blue dots) points from the images of panels a–c, respectively. The soma is marked by a red circle at the origin. F is the formula for ‘flattening’ ratio, F = (a − b)/a (a is the length of the semi-major axis in the projections; b is its semi-minor axis). g Angular distribution in the x–y plane of the dendritic branch and the end points for 5 normal (black), 5 migrated mutant (blue), and 10 non-migrated mutant (red) PC. The plot shows the percentage of the points found in each 10-degree angular interval. The error bars correspond to the SEM. h Flattening ratio of PC projections with the distance from the cerebellar surface (DCS) for 5 normal, 5 migrated mutant (the light blue region), and 10 non-migrated mutant (the pink region: n = 3 for DCS = 200–400 μm; n = 3 for DCS = 400–600 μm; n = 4 for DCS = 600–800 μm) PC. The error bars correspond to the SEM
Mentions: The branching patterns of neurons are critical determinants of connectivity and integration (Greg Stuart and Hausser 1999; Mainen and Sejnowski 1996; Javier and Kreitzer 2012). To quantify the branching patterns of PC dendrites in normal and Crk/CrkL mutant mice, we examined high-resolution microtomographic images. Figure 3a–c shows 3-D volume-rendered images of PC from normal mice, as well as those representing migrated and non-migrated PC from Crk/CrkL mutant mice. The elaborate planar dendritic structure of PC was clearly detected in normal cerebellum using this method (Fig. 3a; Movie S6). Interestingly, migrated PC in Crk/CrkL mutant mice also displayed this characteristic planar feature (Fig. 3b; Movie S7); however, in non-migrated PC, dendrites were distributed in a conical array lacking any planar orientation (Fig. 3c; Movie S8). The 3-D volume-rendered images in Fig. 3a–c were used to calculate branch points and dendrite end points, which were projected as green and blue dots, respectively in Fig. 3d–f. In the case of normal PC and migrated PC in Crk/CrkL mutant mice, projections aligned along the y-axis, indicating a sagittal planar dendritic structure. In contrast, in non-migrated PC, no planar features were evident and dendrites were distributed randomly in the x–y plane. To quantitate the degree of planarity of the normal, we applied a formula for assessing the ‘flattening’ ratio, F = (a − b)/a (a is the length of the semi-major axis in the projections; b is its semi-minor axis). The flattening ratio was high in migrated mutant PC (F = 0.81), similar to that in normal PC (F = 0.90), but it was significantly reduced in non-migrated PC (F = 0.20).Fig. 3

Bottom Line: Purkinje cells that failed to migrate completely exhibited conical dendrites with abnormal 3-D arborization and reduced dendritic complexity.In contrast, Purkinje cells that migrated successfully displayed planar dendritic and spine morphologies similar to normal cells, despite reduced dendritic complexity.While Reelin signaling is important for the migration process, it does not make a direct major contribution to dendrite formation.

View Article: PubMed Central - PubMed

Affiliation: X-ray Imaging Center, School of Interdisciplinary Bioscience and Bioengineering, Pohang University of Science and Technology (POSTECH), Pohang, 790-784, South Korea.

ABSTRACT
The dendritic planarity of Purkinje cells is critical for cerebellar circuit formation. In the absence of Crk and CrkL, the Reelin pathway does not function resulting in partial Purkinje cell migration and defective dendritogenesis. However, the relationships among Purkinje cell migration, dendritic development and Reelin signaling have not been clearly delineated. Here, we use synchrotron X-ray microscopy to obtain 3-D images of Golgi-stained Purkinje cell dendrites. Purkinje cells that failed to migrate completely exhibited conical dendrites with abnormal 3-D arborization and reduced dendritic complexity. Furthermore, their spines were fewer in number with a distorted morphology. In contrast, Purkinje cells that migrated successfully displayed planar dendritic and spine morphologies similar to normal cells, despite reduced dendritic complexity. These results indicate that, during cerebellar formation, Purkinje cells migrate into an environment that supports development of dendritic planarity and spine formation. While Reelin signaling is important for the migration process, it does not make a direct major contribution to dendrite formation.

No MeSH data available.


Related in: MedlinePlus