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A multivariate approach to structural heterogeneity of retinal ganglion cells

Published online by Cambridge University Press:  22 December 2011

I.I. PUSHCHIN*
Affiliation:
Laboratory of Physiology, A.V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
T.A. PODUGOLNIKOVA
Affiliation:
Laboratory for Sensory Information Processing, A.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, AI1 Moscow, Russia
S.L. KONDRASHEV
Affiliation:
Laboratory of Physiology, A.V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
*
*Address correspondence and reprint requests to: I.I. Pushchin, Laboratory of Physiology, A.V. Zhirmunsky Institute of Marine Biology FEB RAS, 17 Palchevskogo Street, Vladivostok 690041, Russia. E-mail: pushchin@imb.dvo.ru

Abstract

Knowing neuronal types is essential for understanding the structural and functional organization of the nervous system. It has long been recognized that neuronal types should be discovered and not defined. This can be done using cluster analysis (CA). Despite there being many studies using CA to classify neurons, only a few of them meet its formal prerequisites. In the present study, we provide an example of using CA in combination with other multivariate techniques for examining neuronal diversity. A special emphasis is put on formal prerequisites to the data and procedure. The data under scrutiny are a sample of ganglion cells projecting to the basal optic nucleus [accessory optic system-projecting ganglion cells (AOS GCs)] in the common frog. There is physiological evidence that these cells comprise at least two functional types but their structural heterogeneity has not been addressed. Cells were labeled with horseradish peroxidase in vivo and examined in whole-mounted retinae using light microscopy. A sample of well-stained cells was obtained and used to estimate 18 structural parameters. A variety of clustering algorithms were used to classify the cells. The joint polar distribution of dendrite mass was monomodal. CA did not reveal a statistically reliable cluster structure in the sample. The clusters were not cohesive and well isolated. ANOVA-on-Ranks revealed no significant between-cluster differences. Our formal conclusion is that functionally distinct frog AOS GCs do not differ in morphology or dendritic arbor orientation. The advantages and limitations of the adopted approach are discussed.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2011

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References

Bajgier, S.M. & Aggarwal, L.K. (1991). Powers of goodness-of-fit tests in detecting balanced mixed normal distributions. Educational and Psychological Measurement 51, 253269.CrossRefGoogle Scholar
Bastakov, V.A., Orlov, O.Yu. & Panyutin, A.K. (1992). Direction-selective retinal ganglion cells projecting to the accessory optic system in the frog Rana temporaria. Sensornye Sistemy 6, 2325.Google Scholar
Bellintani-Guardia, B. & Ott, M. (2002). Displaced retinal ganglion cells project to the accessory optic system in the chameleon (Chamaeleo calyptratus). Experimental Brain Research 145, 5663.CrossRefGoogle Scholar
Bloomfield, S.A. (1994). Orientation-sensitive amacrine and ganglion cells in the rabbit retina. Journal of Neurophysiology 71, 16721691.CrossRefGoogle ScholarPubMed
Bowling, D.B. (1980). Light responses of ganglion cells in the retina of the turtle. The Journal of Physiology 299, 173196.CrossRefGoogle ScholarPubMed
Cook, J.E. (2003). Spatial regularity among retinal neurons. In The Visual Neuroscience, ed. Chalupa, L.M. & Werner, J.S., pp. 463479. Cambridge, MA: MIT Press.CrossRefGoogle Scholar
Cook, J.E. & Podugolnikova, T.A. (2001). Evidence for spatial regularity among retinal ganglion cells that project to the accessory optic system in a frog, a reptile, a bird, and a mammal. Visual Neuroscience 18, 289297.CrossRefGoogle Scholar
Costa, L.D. & Velte, T.J. (1999). Automatic characterization and classification of ganglion cells from the salamander retina. The Journal of Comparative Neurology 404, 3351.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Costello, A.B. & Osborne, L.W. (2005). Best practices in exploratory factor analysis: Four recommendations for getting the most from your analysis. Practical Assessment, Research and Evaluation 10, 19.Google Scholar
Davis, J.C. (2002). Statistics and Data Analysis in Geology. London: John Wiley & Sons.Google Scholar
Deplano, S. & Pedemonte, N. (2002). Spatial organization of displaced ganglion cells in the chick retina. Visual Neuroscience 19, 727734.CrossRefGoogle ScholarPubMed
De Soete, G. (1986). Optimal variable weighting for ultrametric and additive tree clustering. Quality and Quantity 20, 169180.CrossRefGoogle Scholar
De Soete, G. (1998). OVWTRE: A program for optimal variable weighting for ultrametric and additive tree fitting. Journal of Classification 5, 101104.CrossRefGoogle Scholar
Ertöz, L., Steinbach, M. & Kumar, V. (2001). A new Shared nearest neighbor clustering algorithm and its applications. In Workshop on Clustering High Dimensional Data and Its Applications at 2nd SIAM International Conference on Data Mining, Arlington.Google Scholar
Friedman, J.H. & Meulman, J.J. (2004). Clustering objects on subsets of attributes. Journal of the Royal Statistical Society. Series B, Statistical Methodology 66, 815839.CrossRefGoogle Scholar
Giolli, R.A., Blanks, R.H. & Lui, F. (2005). The accessory optic system: Basic organization with an update on connectivity, neurochemistry, and function. Progress in Brain Research 151, 407440.CrossRefGoogle Scholar
Gordon, A.D. (1999). Classification. Boca Raton, FL: Chapman & Hall/CRC.CrossRefGoogle Scholar
Harris, R.M. (1985). Light microscopic depth measurements of thick sections. Journal of Neuroscience Methods 14, 97100.CrossRefGoogle ScholarPubMed
He, S.G. & Masland, R.H. (1998). ON direction-selective ganglion cells in the rabbit retina: Dendritic morphology and pattern of fasciculation. Visual Neuroscience 15, 369375.CrossRefGoogle ScholarPubMed
Hitchcock, P.F. (1989). Exclusionary dendritic interactions in the retina of the goldfish. Development 106, 589598.CrossRefGoogle ScholarPubMed
Hitchcock, P.F. & Easter, S.S. (1986). Retinal ganglion cells in goldfish: A qualitative classification into four morphological types, and a quantitative study of the development of one of them. The Journal of Neuroscience 6, 10371050.CrossRefGoogle Scholar
Jain, A.K. & Dubes, R.C. (1988). Algorithms for Clustering Data. Englewood Cliffs, NJ: Prentice-Hall.Google Scholar
Jelinek, H.F. & Fernández, E. (1998). Neurons and fractals: How reliable and useful are calculations of fractal dimensions? Journal of Neuroscience Methods 81, 918.CrossRefGoogle ScholarPubMed
Kalinina, A.V. & Zhukov, V.A. (1985). Asymmetry in the structure of average and large neurons of the ganglion layer of the frog retina. Neirofiziologiia 17, 456462.Google ScholarPubMed
Karpenko, A.A. (1993). The method and device for the registration of the TV signals from biological objects. Patent of Russia N 1838893 A`3. Informatsionnyi Byulleten’ 32, 46.Google Scholar
Kaufman, L. & Rousseeuw, P.J. (1990). Finding Groups in Data: An Introduction to Cluster Analysis. New York: John Wiley & Sons.CrossRefGoogle Scholar
Kittila, C.A. & Granda, A.M. (1994). Functional morphologies of retinal ganglion cells in the turtle. The Journal of Comparative Neurology 350, 623645.CrossRefGoogle ScholarPubMed
Kondrashev, S.L. & Orlov, O.Y. (1976). Direction-sensitive neurons in the frog visual system. Neurophysiology 8, 159161.CrossRefGoogle Scholar
Kong, J.H., Fish, D.R., Rockhill, R.L. & Masland, R.H. (2005). Diversity of ganglion cells in the mouse retina: Unsupervised morphological classification and its limits. The Journal of Comparative Neurology 489, 293310.CrossRefGoogle ScholarPubMed
Makarenkov, V. & Legendre, P. (2001). Optimal variable weighting for ultrametric and additive trees and K-means partitioning: Methods and software. Journal of Classification 18, 245271.CrossRefGoogle Scholar
Mangrum, W.I., Dowling, J.E. & Cohen, E.D. (2002). A morphological classification of ganglion cells in the zebrafish retina. Visual Neuroscience 19, 767779.CrossRefGoogle ScholarPubMed
Masland, R.H. & Raviola, E. (2000). Confronting complexity: Strategies for understanding the microcircuitry of the retina. Annual Review of Neuroscience 23, 249284.CrossRefGoogle ScholarPubMed
Milligan, G.W. (1996). Clustering validation: Results and implications for applied analyses. In Clustering and Classification, ed. Arabie, P., Hubert, L.J. & De Soete, G., pp. 341375. River Edge, NJ: World Scientific.CrossRefGoogle Scholar
Montgomery, N., Fite, K.V. & Bengston, L. (1981). The accessory optic system of Rana pipiens: Neuroanatomical connections and intrinsic organization. The Journal of Comparative Neurology 203, 595612.CrossRefGoogle ScholarPubMed
Myatt, D.R., Nasuto, S.J. & Maybank, S.J. (2006). Towards the automatic reconstruction of dendritic trees using particle filters. In Proceedings of Nonlinear Statistical Signal Processing Workshop, Cambridge.Google Scholar
Nowak, L.G., Azouz, R., Sanchez-Vives, M.V., Gray, C.M. & McCormick, D.A. (2003). Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. Journal of Neurophysiology 89, 15411566.CrossRefGoogle ScholarPubMed
Oyster, C.W. (1968). The analysis of image motion by the rabbit retina. The Journal of Physiology 199, 613635.CrossRefGoogle ScholarPubMed
Oyster, C.W. & Barlow, H. (1967). Direction-selective units in rabbit retina: Distribution of preferred directions. Science 155, 841842.CrossRefGoogle ScholarPubMed
Pennartz, C.M.A., De Jeu, M.T.G., Geurtsen, A.M.S., Sluiter, A.A. & Hermes, M.L.H.J. (1998). Electrophysiological and morphological heterogeneity of neurons in slices of rat suprachiasmatic nucleus. The Journal of Physiology 506, 775793.CrossRefGoogle ScholarPubMed
Podugolnikova, T.A., Kondrashev, S.L. & Pushchin, I.I. (2007). Morphology of retinal ganglion cells pertaining to the accessory optic system in the common frog Rana temporaria. Sensornye Sistemy 21, 130139.Google Scholar
Podugolnikova, T.A., Orlov, O.Yu. & Reuter, T. (1992 a). Morphology of retinal ganglion cells projecting to the basal optic neuropil in frog. Sensornye Sistemy 5, 2133.Google Scholar
Podugolnikova, T.A., Orlov, O.Yu., Reuter, T. & Mecke, E. (1992 b). Spatial arrangement of retinal ganglion cells pertaining to the accessory optic system in the common frog Rana temporaria. Sensornye Sistemy 6, 2732.Google Scholar
Reiner, A., Brecha, N. & Karten, H.J. (1979). A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken. Neuroscience 4, 16791688.CrossRefGoogle Scholar
Rodieck, R.W. & Brening, R. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior and Evolution 23, 121164.CrossRefGoogle ScholarPubMed
Rousseeuw, P.J. (1987). Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. Journal of Computational and Applied Mathematics 20, 5365.CrossRefGoogle Scholar
Schweitzer, L. & Renehan, W.E. (1997). The use of cluster analysis for cell typing. Brain Research. Brain Research Protocols 1, 100108.CrossRefGoogle ScholarPubMed
Scorcioni, R., Polavaram, S. & Ascoli, G.A. (2008). L-Measure: A web-accessible tool for the analysis, comparison and search of digital reconstructions of neuronal morphologies. Nature Protocols 3, 866876.CrossRefGoogle ScholarPubMed
Sheskin, D.J. (2000). Handbook of Parametric and Nonparametric Statistical Procedures. London: Chapman & Hall/CRC.Google Scholar
Smith, T.G., Marks, W.B., Lange, G.D., Sheriff, W.H. & Neale, E.A. (1989). A fractal analysis of cell images. Journal of Neuroscience Methods 27, 173180.CrossRefGoogle ScholarPubMed
Sokal, R.R. & Rohlf, F.J. (1962). The comparison of dendrograms by objective methods. Taxon 11, 3340.CrossRefGoogle Scholar
Sun, W., Deng, Q., Levick, W.R. & He, S. (2006). ON direction-selective ganglion cells in the mouse retina. The Journal of Physiology 576, 197202.CrossRefGoogle ScholarPubMed
Überla, K. (1977). Faktorenanalyse. Berlin, Germany: Springer-Verlag.Google Scholar
Uchiyama, H., Kanaya, T. & Sonohata, S. (2000). Computation of motion direction by quail retinal ganglion cells that have a nonconcentric receptive field. Visual Neuroscience 17, 263271.CrossRefGoogle ScholarPubMed
Vaney, D.I., He, S., Taylor, W.R. & Levick, W.R. (2001). Direction-selective ganglion cells in the retina. In Motion Vision - Computational, Neural, and Ecological Constraints, ed. Zanker, J.M. & Zeil, J., pp. 1456. Berlin-Heidelberg, Germany: Springer.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447480.CrossRefGoogle ScholarPubMed
Wylie, D.R. & Frost, B.J. (1990). The visual response properties of neurons in the nucleus of the basal optic root of the pigeon: A quantitative analysis. Experimental Brain Research 82, 327336.CrossRefGoogle ScholarPubMed
Yonehara, K., Ishikane, H., Sakuta, H., Shintani, T., Nakamura-Yonehara, K., Kamiji, N. L., Usui, S. & Noda, M. (2009). Identification of retinal ganglion cells and their projections involved in central transmission of information about upward and downward image motion. PLoS One 4, e4320.CrossRefGoogle ScholarPubMed
Zhang, D. & Eldred, W.D. (1994). Anatomical characterization of retinal ganglion cells that project to the nucleus of the basal optic root in the turtle (Pseudemys scripta elegans). Neuroscience 61, 707718.CrossRefGoogle Scholar