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The somal patterning of the AII amacrine cell mosaic in the mouse retina is indistinguishable from random simulations matched for density and constrained by soma size

Published online by Cambridge University Press:  31 January 2018

PATRICK W. KEELEY  and
BENJAMIN E. REESE
PATRICK W. KEELEY
Affiliation:
Neuroscience Research Institute, University of California at Santa Barbara, Santa Barbara, California 93106-5060
BENJAMIN E. REESE*
Affiliation:
Neuroscience Research Institute, University of California at Santa Barbara, Santa Barbara, California 93106-5060 Department of Psychological & Brain Sciences, University of California at Santa Barbara, Santa Barbara, California 93106-9660
*
*Address correspondence to: Benjamin E. Reese, Neuroscience Research Institute, University of California, Santa Barbara, CA 93106-5060. E-mail: [email protected]
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Abstract

The orderly spacing of retinal neurons is commonly regarded as a characteristic feature of retinal nerve cell populations. Exemplars of this property include the horizontal cells and the cholinergic amacrine cells, where individual cells minimize the proximity to like-type neighbors, yielding regularity in the patterning of their somata. Recently, two types of retinal bipolar cells in the mouse retina were shown to exhibit an order in their somal patterning no different from density-matched simulations constrained by soma size but being otherwise randomly distributed. The present study has now extended this finding to a type of retinal amacrine cell, the AII amacrine cell. Voronoi domain analysis revealed the patterning in the population of AII amacrine somata to be no different from density-matched and soma-size-constrained random simulations, while analysis of the density recovery profile showed AII amacrine cells to exhibit a minimal intercellular spacing identical to that for those random simulations: AII amacrine somata were positioned side-by-side as often as chance would predict. Regularity indexes and packing factors (PF) were far lower than those achieved by either the horizontal cells or cholinergic amacrine cells, with PFs also being comparable to those derived from the constrained random simulations. These results extend recent findings that call into question the widespread assumption that all types of retinal neurons are assembled as regular somal arrays, and have implications for the way in which AII amacrine cells must distribute their processes to ensure a uniform coverage of the retinal surface.

Keywords

Prox1Regularity indexNearest neighborVoronoi domainEffective radiusDensity recovery profilePacking factor
Type
Brief Communication
Information
Visual Neuroscience , Volume 35 , 2018 , E003
Copyright
Copyright © Cambridge University Press 2018 

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References

Casini, G., Rickman, D.W. & Brecha, N.C. (1995). AII amacrine cell population in the rabbit retina: Identification by parvalbumin immunoreactivity. Journal of Comparative Neurology 356, 132–142.Google Scholar
Cook, J.E. (1996). Spatial properties of retinal mosaics: An empirical evaluation of some existing measures. Visual Neuroscience 13, 15–30.Google Scholar
Cook, J.E. (1998). Getting to grips with neuronal diversity: What is a neuronal type? In Development and Organization of the Retina, ed. Chalupa, L. & Finlay, B., pp. 91–120. New York: Plenum Press.Google Scholar
Cook, J.E. (2003). Spatial regularity among retinal neurons. In The Visual Neurosciences, ed. Chalupa, L.M. & Werner, J.S., pp. 463–477. Cambridge: MIT Press.Google Scholar
Demb, J.B. & Singer, J.H. (2012). Intrinsic properties and functional circuitry of the AII amacrine cell. Visual Neuroscience 29, 51–60.Google Scholar
Dyer, M.A., Livesey, F.J., Cepko, C.L. & Oliver, G. (2003). Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nature Genetics 34, 53–58.Google Scholar
Eglen, S.J. & Willshaw, D.J. (2002). Influence of cell fate mechanisms upon retinal mosaic formation: A modelling study. Development 129, 5399–5408.Google Scholar
Gaillard, F., Kuny, S. & Sauve, Y. (2014). Retinal distribution of Disabled-1 in a diurnal murine rodent, the Nile grass rat Arvicanthis niloticus . Experimental Eye Research 125, 236–243.Google Scholar
Galli-Resta, L., Novelli, E., Kryger, Z., Jacobs, G.H. & Reese, B.E. (1999). Modelling the mosaic organization of rod and cone photoreceptors with a minimal-spacing rule. European Journal of Neuroscience 11, 1461–1469.Google Scholar
Jeon, Y-K., Kim, T-J., Lee, J-Y., Choi, J-S. & Jeon, C-J. (2007). AII amacrine cells in the inner nuclear layer of bat retina: Identification by parvalbumin immunoreactivity. NeuroReport 18, 1095–1099.Google Scholar
Keeley, P.W., Kim, J.J., Lee, S.C., Haverkamp, S. & Reese, B.E. (2017). Random spatial patterning of cone bipolar cell mosaics in the mouse retina. Visual Neuroscience 34, 1–11.Google Scholar
Keeley, P.W. & Reese, B.E. (2014). The patterning of retinal horizontal cells: Normalizing the regularity index enhances the detection of genomic linkage. Frontiers in Neuroanatomy 8, 113.Google Scholar
Keeley, P.W. & Reese, B.E. (2018). DNER and NFIA are expressed by developing and mature AII amacrine cells in the mouse retina. Journal of Comparative Neurology 526, 467–479.Google Scholar
Keeley, P.W., Whitney, I.E., Madsen, N.R., St John, A.J., Borhanian, S., Leong, S.A., Williams, R.W. & Reese, B.E. (2014). Independent genomic control of neuronal number across retinal cell types. Developmental Cell 30, 103–109.Google Scholar
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of the cat retina. Science 186, 47–49.Google Scholar
Marc, R.E., Anderson, J.R., Jones, B.W., Sigulinsky, C.L. & Lauritzen, J.S. (2014). The AII amacrine cell connectome: A dense network hub. Frontiers in Neural Circuits 8, 104.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1991). Labeling and distribution of AII amacrine cells in the rabbit retina. Journal of Comparative Neurology 304, 491–501.Google Scholar
Pasteels, B., Rogers, J., Blachier, F. & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 1–16.Google Scholar
Perez de Sevilla Muller, L., Azar, S.S., de los Santos, J. & Brecha, N.C. (2017). Prox1 is a marker for AII amacrine cells in the mouse retina. Frontiers in Neuroanatomy 11, 1–12.Google Scholar
Raven, M.A., Eglen, S.J., Ohab, J.J. & Reese, B.E. (2003). Determinants of the exclusion zone in dopaminergic amacrine cell mosaics. Journal of Comparative Neurology 461, 123–136.Google Scholar
Raven, M.A. & Reese, B.E. (2002). Horizontal cell density and mosaic regularity in pigmented and albino mouse retina. Journal of Comparative Neurology 454, 168–176.Google Scholar
Reese, B.E. (2008). Mosaic architecture of the mouse retina. In Eye, Retina, and Visual Systems of the Mouse, ed. Chalupa, L.M. & Williams, R.W., pp. 147–155. Cambridge: MIT Press.Google Scholar
Reese, B.E. & Keeley, P.W. (2015). Design principles and developmental mechanisms underlying retinal mosaics. Biological Reviews 90, 854–876.Google Scholar
Rice, D.S. & Curran, T. (2000). Disabled-1 is expressed in type AII amacrine cells in the mouse retina. Journal of Comparative Neurology 424, 327–338.Google Scholar
Rockhill, R.L., Euler, T. & Masland, R.H. (2000). Spatial order within but not between types of retinal neurons. Proceedings of the National Academy of Sciences 97, 2303–2307.Google Scholar
Rodieck, R.W. (1991). The density recovery profile: A method for the analysis of points in the plane applicable to retinal studies. Visual Neuroscience 6, 95–111.Google Scholar
Seung, H.S. & Sümbül, U. (2014). Neuronal cell types and connectivity: Lessons from the retina. Neuron 83, 1262–1272.Google Scholar
Strettoi, E., Raviola, E. & Dacheux, R.F. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. Journal of Comparative Neurology 325, 152–168.Google Scholar
Vaney, D.I. (1985). The morphology and topographic distribution of AII amacrine cells in the cat retina. Proceedings of the Royal Society of London 224, 475–488.Google Scholar
Vaney, D.I., Gynther, I.C. & Young, H.M. (1991). Rod-signal interneurons in the rabbit retina: 2. AII amacrine cells. Journal of Comparative Neurology 310, 154–169.Google Scholar
Wässle, H., Grunert, U., Chun, M.H. & Boycott, B.B. (1995). The rod pathway of the macaque monkey retina—identification of AII-amacrine cells with antibodies against calretinin. Journal of Comparative Neurology 361, 537–551.Google Scholar
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society of London B. 200, 441–461.Google Scholar
Whitney, I.E., Keeley, P.W., Raven, M.A. & Reese, B.E. (2008). Spatial patterning of cholinergic amacrine cells in the mouse retina. Journal of Comparative Neurology 508, 1–12.Google Scholar