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Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions.

Huckfeldt RM, Schubert T, Morgan JL, Godinho L, Di Cristo G, Huang ZJ, Wong RO - Nat. Neurosci. (2008)

Bottom Line: Repulsive homotypic interactions underlie such patterns in cell organization in invertebrate neurons.Targeted cell ablation revealed that the vertical neurites engage in homotypic interactions that result in tiling of neighboring cells before the establishment of their dendritic fields.This developmental tiling of transient neurites correlates with the emergence of a nonrandom distribution of the cells and could represent a mechanism that organizes neighbor relationships and territories of neurons before circuit assembly.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Structure, University of Washington, 1959 NE Pacific Street, Seattle, Washington 98195, USA.

ABSTRACT
Sensory neurons with common functions are often nonrandomly arranged and form dendritic territories that show little overlap, or tiling. Repulsive homotypic interactions underlie such patterns in cell organization in invertebrate neurons. It is unclear how dendro-dendritic repulsive interactions can produce a nonrandom distribution of cells and their spatial territories in mammalian retinal horizontal cells, as mature horizontal cell dendrites overlap substantially. By imaging developing mouse horizontal cells, we found that these cells transiently elaborate vertical neurites that form nonoverlapping columnar territories on reaching their final laminar positions. Targeted cell ablation revealed that the vertical neurites engage in homotypic interactions that result in tiling of neighboring cells before the establishment of their dendritic fields. This developmental tiling of transient neurites correlates with the emergence of a nonrandom distribution of the cells and could represent a mechanism that organizes neighbor relationships and territories of neurons before circuit assembly.

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Vertical neurites form territories with minimal and stable overlap(a) A field of P2 horizontal cells was followed over time. Cells were segmented and colorized to allow visualization of the neurites of individual cells.(b-c) Each segmented cell was assigned a two-dimensional territory based on the distribution of its neurites (see Methods). Arrows indicate axon-like processes that were included in the territory assignments. Dark grey areas in (c) indicate overlap between two adjacent territories and black areas represent overlap between three territories. Red dots indicate point of apposition.(d) Individual and mean territory sizes over time (16 cells, 3 retinas).(e) Mean overlap between adjacent territories of pairs of neighboring cells over time (16 cells, 3 retinas).(f) Density recovery profile (histogram) of horizontal cells from P2 (n = 265 cells). Light grey bar indicates the equivalent radius (Rt) of horizontal cell territories at these ages and arrow indicates the effective radius (Re) for the DRP. An example of a spatial auto-correlogram is shown above the DRP; note there is an empty zone within about 20 µm of the central reference point (unshaded circle). Each circle represents a cell body with diameter of 3.8 µm.All scale bars, 15 µm. Error bars = S.E.M.
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Figure 4: Vertical neurites form territories with minimal and stable overlap(a) A field of P2 horizontal cells was followed over time. Cells were segmented and colorized to allow visualization of the neurites of individual cells.(b-c) Each segmented cell was assigned a two-dimensional territory based on the distribution of its neurites (see Methods). Arrows indicate axon-like processes that were included in the territory assignments. Dark grey areas in (c) indicate overlap between two adjacent territories and black areas represent overlap between three territories. Red dots indicate point of apposition.(d) Individual and mean territory sizes over time (16 cells, 3 retinas).(e) Mean overlap between adjacent territories of pairs of neighboring cells over time (16 cells, 3 retinas).(f) Density recovery profile (histogram) of horizontal cells from P2 (n = 265 cells). Light grey bar indicates the equivalent radius (Rt) of horizontal cell territories at these ages and arrow indicates the effective radius (Re) for the DRP. An example of a spatial auto-correlogram is shown above the DRP; note there is an empty zone within about 20 µm of the central reference point (unshaded circle). Each circle represents a cell body with diameter of 3.8 µm.All scale bars, 15 µm. Error bars = S.E.M.

Mentions: When viewed en face, the vertical neurites of P0–3 horizontal cells formed distinct, columnar territories. To better visualize these territories, individual cells were segmented and colorized in three-dimension (see Methods) and assigned two-dimensional territories with a custom dilation-erosion software program (Fig. 4a–c). Territory area and overlap, defined as the percentage of a cell’s territory shared with a neighboring cell, were assessed over time. Changes in the size of an individual cell’s territory could be appreciated over 6 to 8 hour intervals (Fig. 4c), although at a population level, the initial mean area of 1101 ± 71 µm2(mean ± s.e.m.; n = 3 retinas, 16 cells) remained constant (Fig. 4d; 0 hours vs. 6–7 hours: P = 0.64; 0 vs. 12–5 hours: P = 0.60; Wilcoxon signed rank test). Territory overlap was 4.8 ± 0.7% and remained relatively stable over these intervals (Fig. 4e; 0 hours vs. 6–7 hours: P = 0.83; 0 vs. 12–15 hours: P = 0.59). Importantly, even the small amount of overlap reported here is likely to be an overestimate because our territory assignment did not exclude the axon-like processes of horizontal cells observed to project far into, and sometimes beyond, neighboring territories (Fig. 4a–c). Territory area and overlap were thus relatively constant despite extensive changes in individual cell morphology.


Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions.

Huckfeldt RM, Schubert T, Morgan JL, Godinho L, Di Cristo G, Huang ZJ, Wong RO - Nat. Neurosci. (2008)

Vertical neurites form territories with minimal and stable overlap(a) A field of P2 horizontal cells was followed over time. Cells were segmented and colorized to allow visualization of the neurites of individual cells.(b-c) Each segmented cell was assigned a two-dimensional territory based on the distribution of its neurites (see Methods). Arrows indicate axon-like processes that were included in the territory assignments. Dark grey areas in (c) indicate overlap between two adjacent territories and black areas represent overlap between three territories. Red dots indicate point of apposition.(d) Individual and mean territory sizes over time (16 cells, 3 retinas).(e) Mean overlap between adjacent territories of pairs of neighboring cells over time (16 cells, 3 retinas).(f) Density recovery profile (histogram) of horizontal cells from P2 (n = 265 cells). Light grey bar indicates the equivalent radius (Rt) of horizontal cell territories at these ages and arrow indicates the effective radius (Re) for the DRP. An example of a spatial auto-correlogram is shown above the DRP; note there is an empty zone within about 20 µm of the central reference point (unshaded circle). Each circle represents a cell body with diameter of 3.8 µm.All scale bars, 15 µm. Error bars = S.E.M.
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Figure 4: Vertical neurites form territories with minimal and stable overlap(a) A field of P2 horizontal cells was followed over time. Cells were segmented and colorized to allow visualization of the neurites of individual cells.(b-c) Each segmented cell was assigned a two-dimensional territory based on the distribution of its neurites (see Methods). Arrows indicate axon-like processes that were included in the territory assignments. Dark grey areas in (c) indicate overlap between two adjacent territories and black areas represent overlap between three territories. Red dots indicate point of apposition.(d) Individual and mean territory sizes over time (16 cells, 3 retinas).(e) Mean overlap between adjacent territories of pairs of neighboring cells over time (16 cells, 3 retinas).(f) Density recovery profile (histogram) of horizontal cells from P2 (n = 265 cells). Light grey bar indicates the equivalent radius (Rt) of horizontal cell territories at these ages and arrow indicates the effective radius (Re) for the DRP. An example of a spatial auto-correlogram is shown above the DRP; note there is an empty zone within about 20 µm of the central reference point (unshaded circle). Each circle represents a cell body with diameter of 3.8 µm.All scale bars, 15 µm. Error bars = S.E.M.
Mentions: When viewed en face, the vertical neurites of P0–3 horizontal cells formed distinct, columnar territories. To better visualize these territories, individual cells were segmented and colorized in three-dimension (see Methods) and assigned two-dimensional territories with a custom dilation-erosion software program (Fig. 4a–c). Territory area and overlap, defined as the percentage of a cell’s territory shared with a neighboring cell, were assessed over time. Changes in the size of an individual cell’s territory could be appreciated over 6 to 8 hour intervals (Fig. 4c), although at a population level, the initial mean area of 1101 ± 71 µm2(mean ± s.e.m.; n = 3 retinas, 16 cells) remained constant (Fig. 4d; 0 hours vs. 6–7 hours: P = 0.64; 0 vs. 12–5 hours: P = 0.60; Wilcoxon signed rank test). Territory overlap was 4.8 ± 0.7% and remained relatively stable over these intervals (Fig. 4e; 0 hours vs. 6–7 hours: P = 0.83; 0 vs. 12–15 hours: P = 0.59). Importantly, even the small amount of overlap reported here is likely to be an overestimate because our territory assignment did not exclude the axon-like processes of horizontal cells observed to project far into, and sometimes beyond, neighboring territories (Fig. 4a–c). Territory area and overlap were thus relatively constant despite extensive changes in individual cell morphology.

Bottom Line: Repulsive homotypic interactions underlie such patterns in cell organization in invertebrate neurons.Targeted cell ablation revealed that the vertical neurites engage in homotypic interactions that result in tiling of neighboring cells before the establishment of their dendritic fields.This developmental tiling of transient neurites correlates with the emergence of a nonrandom distribution of the cells and could represent a mechanism that organizes neighbor relationships and territories of neurons before circuit assembly.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Structure, University of Washington, 1959 NE Pacific Street, Seattle, Washington 98195, USA.

ABSTRACT
Sensory neurons with common functions are often nonrandomly arranged and form dendritic territories that show little overlap, or tiling. Repulsive homotypic interactions underlie such patterns in cell organization in invertebrate neurons. It is unclear how dendro-dendritic repulsive interactions can produce a nonrandom distribution of cells and their spatial territories in mammalian retinal horizontal cells, as mature horizontal cell dendrites overlap substantially. By imaging developing mouse horizontal cells, we found that these cells transiently elaborate vertical neurites that form nonoverlapping columnar territories on reaching their final laminar positions. Targeted cell ablation revealed that the vertical neurites engage in homotypic interactions that result in tiling of neighboring cells before the establishment of their dendritic fields. This developmental tiling of transient neurites correlates with the emergence of a nonrandom distribution of the cells and could represent a mechanism that organizes neighbor relationships and territories of neurons before circuit assembly.

Show MeSH