Spatial patterning of cholinergic amacrine cells in the mouse retina.

Irene E Whitney, Patrick W Keeley, Mary A Raven, Benjamin E Reese
Author Information
  1. Irene E Whitney: Neuroscience Research Institute and Department of Psychology, University of California, Santa Barbara, California 93106, USA.

Abstract

The two populations of cholinergic amacrine cells in the inner nuclear layer (INL) and the ganglion cell layer (GCL) differ in their spatial organization in the mouse retina, but the basis for this difference is not understood. The present investigation examined this issue in six strains of mice that differ in their number of cholinergic cells, addressing how the regularity, packing, and spacing of these cells varies as a function of strain, layer, and density. The number of cholinergic cells was lower in the GCL than in the INL in all six strains. The nearest neighbor and Voronoi domain regularity indexes as well as the packing factor were each consistently lower for the GCL. While these regularity indexes and the packing factor were largely stable across variation in density, the effective radius was inversely related to density for both the GCL and INL, being smaller and more variable in the GCL. Consequently, despite the lower densities in the GCL, neighboring cells were more likely to be positioned closer to one another than in the higher-density INL, thereby reducing regularity and packing. This difference in the spatial organization of cholinergic cells may be due to the cells in the GCL having been passively displaced by fascicles of optic axons and an expanding retinal vasculature during development. In support of this interpretation, we show such displacement of cholinergic somata relative to their dendritic stalks and a decline in packing efficiency and regularity during postnatal development that is more severe for the GCL.

References

  1. Proc Natl Acad Sci U S A. 2005 Jun 14;102(24):8752-7 [PMID: 15937120]
  2. Vis Neurosci. 2004 Jan-Feb;21(1):13-22 [PMID: 15137578]
  3. Angiogenesis. 2007;10(2):77-88 [PMID: 17322966]
  4. J Comp Neurol. 2007 Dec 10;505(5):539-46 [PMID: 17924572]
  5. J Comp Neurol. 2003 Nov 17;466(3):343-55 [PMID: 14556292]
  6. J Comp Neurol. 2007 Feb 1;500(4):693-707 [PMID: 17154252]
  7. J Neurosci. 2004 Sep 15;24(37):8124-34 [PMID: 15371513]
  8. Vis Neurosci. 2005 Jul-Aug;22(4):461-8 [PMID: 16212703]
  9. Dev Dyn. 2003 Oct;228(2):231-8 [PMID: 14517994]
  10. Nature. 2002 Aug 22;418(6900):845-52 [PMID: 12192402]
  11. Brain Res Dev Brain Res. 1988 Nov 1;44(1):73-85 [PMID: 3069242]
  12. Eur J Neurosci. 2000 Oct;12(10):3819-22 [PMID: 11029653]
  13. Differentiation. 1983;25(2):193-203 [PMID: 6198232]
  14. J Neurosci. 1997 Oct 15;17(20):7831-8 [PMID: 9315903]
  15. Neuron. 1994 Oct;13(4):1017-30 [PMID: 7946326]
  16. J Comp Neurol. 1981 Jul 1;199(3):373-91 [PMID: 6114966]
  17. Vis Neurosci. 1991 Feb;6(2):95-111 [PMID: 2049333]
  18. Neuron. 2006 Sep 21;51(6):787-99 [PMID: 16982423]
  19. Neuron. 2001 Jun;30(3):771-80 [PMID: 11430810]
  20. Vis Neurosci. 1996 Jan-Feb;13(1):15-30 [PMID: 8730986]
  21. J Comp Neurol. 2005 Apr 11;484(3):331-43 [PMID: 15739235]
  22. Cell Tissue Res. 1986;246(1):91-102 [PMID: 3536118]
  23. Glia. 1994 Jan;10(1):40-8 [PMID: 7507886]
  24. Eur J Neurosci. 1999 Aug;11(8):2965-78 [PMID: 10457191]
  25. Invest Ophthalmol Vis Sci. 2009 May;50(5):1996-2003 [PMID: 19168892]
  26. Invest Ophthalmol Vis Sci. 1998 Aug;39(9):1713-20 [PMID: 9699561]
  27. Brain Res. 1987 Nov 17;426(1):119-30 [PMID: 3690309]
  28. J Comp Neurol. 2002 Apr 22;446(1):1-10 [PMID: 11920715]
  29. Vis Neurosci. 2005 Sep-Oct;22(5):569-73 [PMID: 16332267]
  30. Curr Opin Neurobiol. 2002 Aug;12(4):405-10 [PMID: 12139988]
  31. Nature. 2005 Dec 15;438(7070):960-6 [PMID: 16355161]
  32. J Comp Neurol. 2003 Feb 3;456(2):154-66 [PMID: 12509872]
  33. Nature. 1988 Apr 28;332(6167):834-7 [PMID: 3282180]
  34. Cell Tissue Res. 2004 Aug;317(2):109-15 [PMID: 15221444]
  35. Exp Eye Res. 1997 May;64(5):759-66 [PMID: 9245906]
  36. J Comp Neurol. 2000 Nov 27;427(4):604-16 [PMID: 11056467]

Grants

  1. R01 EY011087-09S1/NEI NIH HHS
  2. R01 EY011087-09/NEI NIH HHS
  3. R01 EY011087-07A1/NEI NIH HHS
  4. R01 EY011087-08/NEI NIH HHS
  5. R01 EY011087/NEI NIH HHS
  6. EY-11087/NEI NIH HHS

MeSH Term

Acetylcholine
Amacrine Cells
Animals
Cell Count
Choline O-Acetyltransferase
Glial Fibrillary Acidic Protein
Mice
Mice, Inbred Strains
Neurofilament Proteins
Retina

Chemicals

Glial Fibrillary Acidic Protein
Neurofilament Proteins
neurofilament protein 150
Choline O-Acetyltransferase
Acetylcholine

Word Cloud

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