Abstract
In the developing mammalian retina, horizontal neurons undergo a dramatic reorganization of their processes shortly after they migrate to their appropriate laminar position. This is an important process because it is now understood that the apical processes are important for establishing the regular mosaic of horizontal cells in the retina and proper reorganization during lamination is required for synaptogenesis with photoreceptors and bipolar neurons. However, this process is difficult to study because the analysis of horizontal neuron anatomy is labor intensive and time-consuming. In this paper, we present a computational method for automatically tracing the three-dimensional (3-D) dendritic structure of horizontal retinal neurons in two-photon laser scanning microscope (TPLSM) imagery. Our method is based on 3-D skeletonization and is thus able to preserve the complex structure of the dendritic arbor of these cells. We demonstrate the effectiveness of our approach by comparing our tracing results against two sets of semi-automated traces over a set of 10 horizontal neurons ranging in age from P1 to P5. We observe an average agreement level of 81% between our automated trace and the manual traces. This automated method will serve as an important starting point for further refinement and optimization.
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18 May 2019
The authors regret that they neglected to cite their conference report on the technical part of a ���preliminary study��� presented at, and published in, the Biomedical Sciences and Engineering Conference (BSEC), 2010, May 25-26 (Fully automated segmentation and characterization of the dendritic trees of retinal horizontal neurons -DOI: 10.1109/BSEC.2010.5510843 ), as it related to the larger dataset presented as validation of the method in the Neurochemical Research article (Automated Tracing of Horizontal Neuron Processes During Retinal Development- Neurochem Res. 2011 Apr;36(4):583-93). This resulted in the lack of transparency on the re-use and duplication of introductory text, which should have been cited. No figures or tables were reproduced, but rather larger confirmatory data and different set of results were reported. Appropriate authors were cited in both papers
18 May 2019
The authors regret that they neglected to cite their conference report on the technical part of a ���preliminary study��� presented at, and published in, the Biomedical Sciences and Engineering Conference (BSEC), 2010, May 25-26 (Fully automated segmentation and characterization of the dendritic trees of retinal horizontal neurons -DOI: 10.1109/BSEC.2010.5510843 ), as it related to the larger dataset presented as validation of the method in the Neurochemical Research article (Automated Tracing of Horizontal Neuron Processes During Retinal Development- Neurochem Res. 2011 Apr;36(4):583-93). This resulted in the lack of transparency on the re-use and duplication of introductory text, which should have been cited. No figures or tables were reproduced, but rather larger confirmatory data and different set of results were reported. Appropriate authors were cited in both papers
References
Livesey FJ, Cepko CL (2001) Vertebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2:109–118
Donovan SL, Dyer MA (2005) Regulation of proliferation during central nervous system development. Semin Cell Dev Biol 16:407–421
Cepko CL, Austin CP, Yang X et al (1996) Cell fate determination in the vertebrate retina. Proc Natl Acad Sci USA 93:589–595
Dyer MA (2003) Regulation of proliferation, cell fate specification and differentiation by the homeodomain proteins Prox1, Six3, and Chx10 in the developing retina. Cell Cycle 2:350–357
Dyer MA, Cepko CL (2001) Regulating proliferation during retinal development. Nat Rev Neurosci 2:333–342
Belliveau MJ, Cepko CL (1999) Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina. Development 126:555–566
Donovan SL, Dyer MA (2004) Developmental defects in Rb-deficient retinae. Vision Res 44:3323–3333
Johnson DA, Donovan SL, Dyer MA (2006) Mosaic deletion of Rb arrests rod differentiation and stimulates ectopic synaptogenesis in the mouse retina. J Comp Neurol 498:112–128
Al-Kofahi O, Radke RJ, Roysam B et al (2006) Automated semantic analysis of changes in image sequences of neurons in culture. IEEE Trans Biomed Eng 53:1109–1123
Xiong G, Zhou X, Degterev A et al (2006) Automated neurite labeling and analysis in fluorescence microscopy images. Cytometry A 69:494–505
Lee PC, Ching YT, Chang HM, Chiang AS (2008) A semi-automatic method for neuron centerline extraction in confocal microscopic image stack. IEEE International Symposium on Biomedical Imaging 5, 3
Losavio BE et al (2008) Live neuron morphology automatically reconstructed from multiphoton and confocal imaging data. J Neurophysiol 100:2422–2429
Chan TF, Vese LA (2001) Active contours without edges. IEEE Trans Image Process 10:266–277
Chen Z, Molloi S (2003) Automatic 3D vascular tree construction in CT angiography. Comput Med Imaging Graph 27:469–479
Borgefors G, Nyström I, Di Baja GS (1999) Computing skeletons in three dimensions. Pattern Recogn 32:1225–1236
Ma CM, Sonka M (1996) A fully parallel 3D thinning algorithm and its applications. Comput Vision Image Underst 64:420–433
He X, Kischell M, Rioult M et al (1998) Three-dimensional thinning algorithm that peels the outmost layer with application to neuron tracing. J Comput Assisted Microsc 10:123–135
Huckfeldt RM, Schubert T, Morgan JL et al (2009) Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nat Neurosci 12:35–43
Dyer MA, Cepko CL (2000) Control of Muller glial cell proliferation and activation following retinal injury. Nat Neurosci 3:873–880
Jones BW et al (2003) Retinal remodeling triggered by photoreceptor degenerations. J Comp Neurol 464:1–16
Marc RE, Jones BW (2003) Retinal remodeling in inherited photoreceptor degenerations. Mol Neurobiol 28:139–147
Marc RE, Jones BW, Watt CB et al (2003) Neural remodeling in retinal degeneration. Prog Retin Eye Res 22:607–655
Acknowledgments
Supported by grants from the National Institutes of Health (R01EY018599 and R01EY014867); Cancer Center Support CA 21765 from the National Cancer Institute; and grants from the American Cancer Society, the Pew Charitable Trust, Macular Vision Research Foundation and the American Lebanese Syrian Associated Charities. Dr. Dyer is a Howard Hughes Medical Institute Early Career Investigator.
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Special Issue: In Honor of Dr. Dianna Johnson.
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Kerekes, R.A., Martins, R.A.P., Davis, D. et al. Automated Tracing of Horizontal Neuron Processes During Retinal Development. Neurochem Res 36, 583–593 (2011). https://doi.org/10.1007/s11064-010-0390-1
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DOI: https://doi.org/10.1007/s11064-010-0390-1