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Cone and rod cells have different target preferences in vitro as revealed by optical tweezers.

Clarke RJ, Högnason K, Brimacombe M, Townes-Anderson E - Mol. Vis. (2008)

Bottom Line: Cell orientation of the photoreceptor also did not affect preferences: Cells oriented away from dendritic processes could reorient their axonal pole toward the target cell.Cone cells preferred normal partners, and rod cells preferred novel partners.Further,these differences may help explain the patterns of photoreceptor sprouting seen in retinal degeneration in which rod, but not cone, cells invade the inner retinal layers where third-order neurons are located.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology and Neuroscience, New Jersey Medical School, University of Medicine and Dentistry of New Jersey, Newark, NJ 07103, USA.

ABSTRACT

Purpose: When neural circuits are damaged in adulthood, regenerating and sprouting processes must distinguish appropriate targets to recreate the normal circuitry. We tested the ability of adult nerve cells to target specific cells in culture using the retina as a model system.

Methods: Under sterile culture conditions, retinal cells, isolated from tiger salamander retina, were micromanipulated with optical tweezers to create pairs of first-order photoreceptor cells with second- or third-order retinal neurons. The development of cell contact and presynaptic varicosities, the direction and amount of neuritic growth, and nerve cell polarity were assessed after seven days in vitro. Cultures were labeled for rod opsin to distinguish rod from cone cells and for the alpha subunit of the trimeric G protein Go (Go alpha) to identify cone-dominated and mixed rod-cone ON bipolar cells.

Results: Quantitative analysis of growth demonstrated that target preferences were cell-specific: Cone cells preferred second-order bipolar cells, whereas rod cells grew toward third-order neurons, which include amacrine and ganglion cells. In addition, when rod cells grew toward bipolar cells, they chose an abnormally high number of Go alpha-positive bipolar cells. These growth patterns were not affected by tweezers manipulation or the amount of growth. Cell orientation of the photoreceptor also did not affect preferences: Cells oriented away from dendritic processes could reorient their axonal pole toward the target cell.

Conclusions: Cone cells preferred normal partners, and rod cells preferred novel partners. These intrinsic preferences indicate that adult nerve cells can have differing capacities for targeting even if they come from the same cell class. Further,these differences may help explain the patterns of photoreceptor sprouting seen in retinal degeneration in which rod, but not cone, cells invade the inner retinal layers where third-order neurons are located.

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Varicosity development changes depending on cell pair interactions. A: For cones (n=105) and rods (n=133), the total number of varicosities did not depend on whether there was attraction or repulsion to the paired cell. The trend toward more varicosities in cells attracted to their target was not significant. B: However, the number of varicosities formed by photoreceptors was increased if contact with the target cell was present in one-week cultures (asterisk denotes p<0.05, tested with the Mann–Whitney test). C: Looking at the cone and rod cells separately, the average number of varicosities made by cone cells was significantly increased if contact was made with the target cell (asterisk denotes p<0.05, Mann–Whitney test; the n’s are the same as above). D: For rod cells, but not cones, the number of varicosities was significantly increased with contact when only those cells that made varicosities were analyzed (asterisk denotes p<0.05, Mann–Whitney test). Sixty-two of 105 cone cells had varicosities; 95 of 133 rod cells had varicosities.
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f5: Varicosity development changes depending on cell pair interactions. A: For cones (n=105) and rods (n=133), the total number of varicosities did not depend on whether there was attraction or repulsion to the paired cell. The trend toward more varicosities in cells attracted to their target was not significant. B: However, the number of varicosities formed by photoreceptors was increased if contact with the target cell was present in one-week cultures (asterisk denotes p<0.05, tested with the Mann–Whitney test). C: Looking at the cone and rod cells separately, the average number of varicosities made by cone cells was significantly increased if contact was made with the target cell (asterisk denotes p<0.05, Mann–Whitney test; the n’s are the same as above). D: For rod cells, but not cones, the number of varicosities was significantly increased with contact when only those cells that made varicosities were analyzed (asterisk denotes p<0.05, Mann–Whitney test). Sixty-two of 105 cone cells had varicosities; 95 of 133 rod cells had varicosities.

Mentions: The preferences demonstrated in culture may be influenced by general stimulation or inhibition of photoreceptor growth by potential postsynaptic partners. This would result in greater growth from photoreceptor cells attracted to their partner and possibly less growth with inhibition, which might make it more difficult to detect repulsion. We compared, therefore, the number of varicosities and the number and total length of processes produced by attracted versus repulsed photoreceptors. Surprisingly, repulsive cells did not reduce total photoreceptor growth. Instead, the average number of varicosities (Figure 5A), neurites, and total length of neuritic growth (data not shown) did not differ regardless of whether the cells were attracted to or repulsed by a partner cell. Additionally, qualitative assessment of the amount and direction of growth by target cells suggested that growth by target cells did not determine photoreceptor targeting: abundant growth by target cells toward the photoreceptor could still result in repulsion of photoreceptor growth, whereas no growth by a target cell could result in attraction (compare Figures 2B and 2C).


Cone and rod cells have different target preferences in vitro as revealed by optical tweezers.

Clarke RJ, Högnason K, Brimacombe M, Townes-Anderson E - Mol. Vis. (2008)

Varicosity development changes depending on cell pair interactions. A: For cones (n=105) and rods (n=133), the total number of varicosities did not depend on whether there was attraction or repulsion to the paired cell. The trend toward more varicosities in cells attracted to their target was not significant. B: However, the number of varicosities formed by photoreceptors was increased if contact with the target cell was present in one-week cultures (asterisk denotes p<0.05, tested with the Mann–Whitney test). C: Looking at the cone and rod cells separately, the average number of varicosities made by cone cells was significantly increased if contact was made with the target cell (asterisk denotes p<0.05, Mann–Whitney test; the n’s are the same as above). D: For rod cells, but not cones, the number of varicosities was significantly increased with contact when only those cells that made varicosities were analyzed (asterisk denotes p<0.05, Mann–Whitney test). Sixty-two of 105 cone cells had varicosities; 95 of 133 rod cells had varicosities.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2383278&req=5

f5: Varicosity development changes depending on cell pair interactions. A: For cones (n=105) and rods (n=133), the total number of varicosities did not depend on whether there was attraction or repulsion to the paired cell. The trend toward more varicosities in cells attracted to their target was not significant. B: However, the number of varicosities formed by photoreceptors was increased if contact with the target cell was present in one-week cultures (asterisk denotes p<0.05, tested with the Mann–Whitney test). C: Looking at the cone and rod cells separately, the average number of varicosities made by cone cells was significantly increased if contact was made with the target cell (asterisk denotes p<0.05, Mann–Whitney test; the n’s are the same as above). D: For rod cells, but not cones, the number of varicosities was significantly increased with contact when only those cells that made varicosities were analyzed (asterisk denotes p<0.05, Mann–Whitney test). Sixty-two of 105 cone cells had varicosities; 95 of 133 rod cells had varicosities.
Mentions: The preferences demonstrated in culture may be influenced by general stimulation or inhibition of photoreceptor growth by potential postsynaptic partners. This would result in greater growth from photoreceptor cells attracted to their partner and possibly less growth with inhibition, which might make it more difficult to detect repulsion. We compared, therefore, the number of varicosities and the number and total length of processes produced by attracted versus repulsed photoreceptors. Surprisingly, repulsive cells did not reduce total photoreceptor growth. Instead, the average number of varicosities (Figure 5A), neurites, and total length of neuritic growth (data not shown) did not differ regardless of whether the cells were attracted to or repulsed by a partner cell. Additionally, qualitative assessment of the amount and direction of growth by target cells suggested that growth by target cells did not determine photoreceptor targeting: abundant growth by target cells toward the photoreceptor could still result in repulsion of photoreceptor growth, whereas no growth by a target cell could result in attraction (compare Figures 2B and 2C).

Bottom Line: Cell orientation of the photoreceptor also did not affect preferences: Cells oriented away from dendritic processes could reorient their axonal pole toward the target cell.Cone cells preferred normal partners, and rod cells preferred novel partners.Further,these differences may help explain the patterns of photoreceptor sprouting seen in retinal degeneration in which rod, but not cone, cells invade the inner retinal layers where third-order neurons are located.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology and Neuroscience, New Jersey Medical School, University of Medicine and Dentistry of New Jersey, Newark, NJ 07103, USA.

ABSTRACT

Purpose: When neural circuits are damaged in adulthood, regenerating and sprouting processes must distinguish appropriate targets to recreate the normal circuitry. We tested the ability of adult nerve cells to target specific cells in culture using the retina as a model system.

Methods: Under sterile culture conditions, retinal cells, isolated from tiger salamander retina, were micromanipulated with optical tweezers to create pairs of first-order photoreceptor cells with second- or third-order retinal neurons. The development of cell contact and presynaptic varicosities, the direction and amount of neuritic growth, and nerve cell polarity were assessed after seven days in vitro. Cultures were labeled for rod opsin to distinguish rod from cone cells and for the alpha subunit of the trimeric G protein Go (Go alpha) to identify cone-dominated and mixed rod-cone ON bipolar cells.

Results: Quantitative analysis of growth demonstrated that target preferences were cell-specific: Cone cells preferred second-order bipolar cells, whereas rod cells grew toward third-order neurons, which include amacrine and ganglion cells. In addition, when rod cells grew toward bipolar cells, they chose an abnormally high number of Go alpha-positive bipolar cells. These growth patterns were not affected by tweezers manipulation or the amount of growth. Cell orientation of the photoreceptor also did not affect preferences: Cells oriented away from dendritic processes could reorient their axonal pole toward the target cell.

Conclusions: Cone cells preferred normal partners, and rod cells preferred novel partners. These intrinsic preferences indicate that adult nerve cells can have differing capacities for targeting even if they come from the same cell class. Further,these differences may help explain the patterns of photoreceptor sprouting seen in retinal degeneration in which rod, but not cone, cells invade the inner retinal layers where third-order neurons are located.

Show MeSH
Related in: MedlinePlus