Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach
Abstract
Any investigation of the total number of neurons in a given brain region must first address the following questions. What is the best method for estimating the total number of neurons? What are the validity and the expected precision of the obtained data? What precision must the estimates attain with respect to the scientific question? In the present study, these questions were addressed using a computer simulation. Virtual brain regions with various spatial distributions of virtual neurons were modeled. The total numbers of virtual neurons in the modeled brain regions were repeatedly estimated by simulation of modern design-based stereology, either by using the 'fractionator' method or by the established method based on the product of estimated neuron density and estimated volume of the reference space. We show that estimates of total numbers of neurons obtained using the fractionator are from a statistical and economical standpoint more efficient than corresponding estimates obtained using the density/volume procedure. Furthermore, the use of two simple prediction methods (one for homogeneous and the other for clustered neuron distributions) permits satisfactory predictions about the variation of presumably any estimates of total numbers of neurons obtained using the fractionator. Finally, we show that assessing the reliability of estimates of mean total neuronal numbers using the ratio between the mean of the squared coefficients of error of the estimates and the squared coefficient of variation of the estimated total neuronal numbers, a frequently employed method in stereological studies, is neither useful nor informative. The present results may constitute a new set of recommendations for the rigorous usage of design-based stereology. In particular, we strongly recommend counting considerably more neurons than is currently done in the literature when estimating total neuronal numbers using design-based stereology.
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The average coefficient of error of the optical disector analyses was 0.085 ± 0.018 (mean ± SD).
“On average, the coefficient of error (56) of optical disector analyses was 0.085 ± 0.018 (mean ± SD).”
From Evolution of increased glia–neuron ratios in the human frontal cortex (2006) · cites this paper as [56]
Cites
The Art of Computer Programming
Knuth, D. E. (1968) · Cited by 16,097 · see citing works
The Art of Computer Programming. Volume 2: Seminumerical Algorithms.
Taussky, O., & Knuth, D. E. (1970) · American Mathematical Monthly · doi:10.2307/2317055 · Cited by 3,863 · see citing works
The efficiency of systematic sampling in stereology and its prediction *
Gundersen, H., & Jensen, E. B. V. (1987) · Journal of Microscopy · doi:10.1111/j.1365-2818.1987.tb02837.x · Cited by 3,586 · see citing works
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · see citing works
Statistical analysis of spatial point patterns
(1986) · Environmental Software · doi:10.1016/0266-9838(86)90012-2 · Cited by 2,929 · see citing works
Gundersen, H. J. G., Bagger, P. V., Bendtsen, T. F., Evans, S. M., Korbo, L., Marcussen, N., Møller, A., Nielsen, K. N., Nyengaard, J. R., Pakkenberg, B., et al. (1988) · Apmis · doi:10.1111/j.1699-0463.1988.tb00954.x · Cited by 2,480 · see citing works
Ripley, B. D. (1987) · Wiley Series in Probability and Statistics · doi:10.1002/9780470316726 · Cited by 2,241 · see citing works
Gundersen, H. J. G. (1986) · PubMed · Cited by 1,659 · see citing works
Stereology of arbitrary particles*
Gundersen, H. J. G. (1986) · Journal of Microscopy · doi:10.1111/j.1365-2818.1986.tb02764.x · Cited by 1,444 · see citing works
The efficiency of systematic sampling in stereology—reconsidered
GUNDERSEN, H. J. G., JENSEN, E. B. V., KIÊU, K., & NIELSEN, J. (1999) · Journal of Microscopy · doi:10.1046/j.1365-2818.1999.00457.x · Cited by 1,317 · see citing works
Bronshtein, I. N., Semendyayev, K. A., Musiol, G., & Muehlig, H. (1979) · Springer eBooks · doi:10.1007/978-3-662-05382-9 · Cited by 1,238 · see citing works
Unbiased stereological estimation of the number of neurons in the human hippocampus
West, M. J., & Gundersen, H. J. G. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.902960102 · Cited by 1,153 · cited 5× · see citing works
“(5) (West and Gundersen, 1990): nV×N=6ref×nV (5) To obtain estimates of the average total boundary length of the sections (B( ), a third set of rectangular lattices with uniform side length slB was placed in a systematic–random manner on the upper surface of the sections (Fig.”
BackgroundMethodInfluentialWarde, W. D., Scheaffer, R. L., Mendenhall, W. M., & Ott, L. (1987) · Technometrics · doi:10.2307/1269791 · Cited by 961 · see citing works
New stereological methods for counting neurons
West, M. J. (1993) · Neurobiology of Aging · doi:10.1016/0197-4580(93)90112-o · Cited by 940 · see citing works
Linear Models for Unbalanced Data
Turner, D. D., & Searle, S. R. (1989) · Technometrics · doi:10.2307/1270372 · Cited by 585 · see citing works
Optimizing sampling efficiency of stereological studies in biology: or ‘Do more less well!‘
Gundersen, H. J. G., & Østerby, R. (1981) · Journal of Microscopy · doi:10.1111/j.1365-2818.1981.tb01199.x · Cited by 536 · see citing works
Efficient and portable combined random number generators
L’Ecuyer, P. (1988) · Communications of the ACM · doi:10.1145/62959.62969 · Cited by 494 · see citing works
A review of pseudorandom number generators
James, F. (1990) · Computer Physics Communications · doi:10.1016/0010-4655(90)90032-v · Cited by 464 · see citing works
Stereologic Methods and Their Application in Kidney Research
Nyengaard, J. R. (1999) · Journal of the American Society of Nephrology · doi:10.1681/asn.v1051100 · Cited by 441 · see citing works
Matheron, G. (1965) · Masson et Cie eBooks · Cited by 420 · see citing works
Czaja, R., Scheaffer, R. L., Mendenhall, W. M., & Ott, L. (1987) · Journal of the American Statistical Association · doi:10.2307/2289408 · Cited by 302 · see citing works
Mayhew, T. M., & Gundersen, H. J. G. (1996) · PubMed · Cited by 291 · see citing works
Any way you cut it: A new journal policy for the use of unbiased counting methods
Saper, C. B. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960101)364:1 · Cited by 226 · see citing works
Voronoi tessellation to study the numerical density and the spatial distribution of neurones
Duyckaerts, C. J., & Godefroy, G. (2000) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(00)00064-8 · Cited by 197 · see citing works
Unbiased stereological estimation of the total number of synapses in a brain region
Geinisman, Y., Gundersen, H. J. G., van der Zee, E., & West, M. J. (1996) · Journal of Neurocytology · doi:10.1007/bf02284843 · Cited by 161 · see citing works
Bongiovanni, J. (1988) · Environmental Software · doi:10.1016/0266-9838(88)90009-3 · Cited by 140 · see citing works
Stereology of nerve cross sections
Larsen, J. O. (1998) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(98)00129-0 · Cited by 134 · see citing works
Precision of Cavalieri sections and slices with local errors
Cruz-Orive, L. M. (1999) · Journal of Microscopy · doi:10.1046/j.1365-2818.1999.00460.x · Cited by 130 · see citing works
Variation of fractionator estimates and its prediction
Schmitz, C. (1998) · Anatomy and Embryology · doi:10.1007/s004290050191 · Cited by 129 · see citing works
Self-citationWagner, C. K., & Morrell, J. I. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960617)370:1 · Cited by 125 · see citing works
Glaser, E. M., & Wilson, P. D. (1998) · Journal of Microscopy · doi:10.1046/j.1365-2818.1998.00417.x · Cited by 122 · see citing works
Cruz-Orive, L. M. (1997) · Journal of Microscopy · doi:10.1046/j.1365-2818.1997.1380695.x · Cited by 116 · see citing works
Linear Models for Unbalanced Data.
Boik, R. J., & Searle, S. R. (1988) · Journal of the American Statistical Association · doi:10.2307/2289336 · Cited by 105 · see citing works
Estimation of fetal volume by magnetic resonance imaging and stereology
Roberts, N., Garden, A., Cruz-Orive, L. M., Whitehouse, G. H., & Edwards, R. H. T. (1994) · British Journal of Radiology · doi:10.1259/0007-1285-67-803-1067 · Cited by 103 · see citing works
Nerve cell loss in the thalamic mediodorsal nucleus in Huntington's disease
Heinsen, H., Rüb, U., Bauer, M., Ulmar, G., Bethke, B., Schüler, M., Böcker, F. M., Eisenmenger, W., Götz, M., Korr, H., et al. (1999) · Acta Neuropathologica · doi:10.1007/s004010051037 · Cited by 102 · see citing works
Self-citationHeinsen, H., Arzberger, T., & Schmitz, C. (2000) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(00)00067-3 · Cited by 94 · see citing works
Self-citationKönig, D., Carvajal‐Gonzalez, S., Downs, A. M., Vassy, J., & Rigaut, P. (1991) · Journal of Microscopy · doi:10.1111/j.1365-2818.1991.tb03100.x · Cited by 59 · see citing works
Application of Statistical Methods in Quantitative Microscopy*
Nicholson, W. L. (1978) · Journal of Microscopy · doi:10.1111/j.1365-2818.1978.tb00102.x · Cited by 58 · see citing works
On the empirical variance of a fractionator estimate
Cruz-Orive, L. M. (1990) · Journal of Microscopy · doi:10.1111/j.1365-2818.1990.tb03050.x · Cited by 48 · see citing works
Schmitz, C., Rüb, U., Korr, H., & Heinsen, H. (1999) · Acta Neuropathologica · doi:10.1007/s004010051038 · Cited by 27 · see citing works
Self-citationNeuron loss in the mouse hippocampus following prenatal injection of tritiated thymidine or saline
Schmitz, C., Bültmann, E., Gube, M., & Korr, H. (1999) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(99)00029-5 · Cited by 27 · see citing works
Self-citationNo loss of hippocampal neurons in AIDS patients
Korbo, L., & West, M. J. (2000) · Acta Neuropathologica · doi:10.1007/s004010051156 · Cited by 22 · see citing works
Begega, A., Cuesta, M., Santín, L. J., Rubio, S., Astudillo, A., & Arias, J. L. (1999) · Experimental Gerontology · doi:10.1016/s0531-5565(99)00048-0 · Cited by 22 · see citing works
Toward a more objective biology
Cruz-Orive, L. M. (1994) · Neurobiology of Aging · doi:10.1016/0197-4580(94)90039-6 · Cited by 22 · see citing works
Don't dissect use the disector!
Maynard, R. L. (1996) · Human & Experimental Toxicology · doi:10.1177/096032719601501015 · Cited by 22 · see citing works
Towards more readily comprehensible procedures in disector stereology
Schmitz, C. (1997) · Journal of Neurocytology · doi:10.1023/a:1018506113256 · Cited by 19 · see citing works
Self-citationEvaluation of the precision of systematic sampling: Nugget effect and covariogram modelling
Thioulouse, J., Royet, J., Ploye, H., & Houllier, F. (1993) · Journal of Microscopy · doi:10.1111/j.1365-2818.1993.tb03419.x · Cited by 18 · see citing works
Reed, M., & Howard, C. V. (1997) · Journal of Microscopy · doi:10.1046/j.1365-2818.1997.1710741.x · Cited by 16 · see citing works
Towards the use of state-of-the-art stereology in experimental gerontology
Schmitz, C. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00094-2 · Cited by 8 · see citing works
Self-citationMcShane, L. M., & Palmatier, M. A. (1994) · Statistics in Medicine · doi:10.1002/sim.4780130515 · Cited by 5 · see citing works
Glaser, E. M., & Wilson, P. D. (1999) · Image Analysis & Stereology · Cited by 4 · see citing works
Wang (1996) · doi:10.1002/(sici)1096-9861(19960318)366:4
?imi?, G., Kostovi?, I., Winblad, B., & Bogdanovi?, N. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970324)379:4
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von Bartheld, C. S., Bahney, J., & Herculano‐Houzel, S. (2016) · Journal of Comparative Neurology · doi:10.1002/cne.24040 · Cited by 1,063 · see citing works
Design-based stereology in neuroscience
Schmitz, C., & Hof, P. R. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.08.050 · Cited by 676 · see citing works
Self-citationKellendonk, C., Simpson, E. H., Polan, H. J., Malleret, G., Vronskaya, S., Winiger, V., Moore, H., & Kandel, E. R. (2006) · Neuron · doi:10.1016/j.neuron.2006.01.023 · Cited by 520 · see citing works
Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms
Andorfer, C., Acker, C. M., Kress, Y., Hof, P. R., Duff, K., & Davies, P. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4637-04.2005 · Cited by 511 · see citing works
“The coefficient of error was calculated according to Schmitz and Hof (2000).”
MethodSelf-citationHof, P. R., Haroutunian, V., Friedrich, V. L., Byne, W., Buitron, C., Perl, D. P., & Davis, K. L. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00237-3 · Cited by 433 · see citing works
Self-citationCasas, C., Sergeant, N., Itier, J.-M., Blanchard, V., Wirths, O., van der Kolk, N., Vingtdeux, V., van de Steeg, E., Ret, G., Canton, T., et al. (2004) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63388-3 · Cited by 400 · see citing works
Self-citationChu, Y., & Kordower, J. H. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.08.021 · Cited by 396 · see citing works
Early frontotemporal dementia targets neurons unique to apes and humans
Seeley, W. W., Carlin, D. A., Allman, J. M., Macedo, M. N., Bush, C., Miller, B. L., & DeArmond, S. J. (2006) · Annals of Neurology · doi:10.1002/ana.21055 · Cited by 364 · see citing works
Evolution of increased glia–neuron ratios in the human frontal cortex
Sherwood, C. C., Stimpson, C. D., Raghanti, M. A., Wildman, D. E., Uddin, M., Grossman, L. I., Goodman, M., Redmond, J. C., Bonar, C. J., Erwin, J. M., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605843103 · Cited by 342 · see citing works
Self-citationSchmitz, C., Rutten, B. P. F., Pielen, A., Schäfer, S., Wirths, O., Tremp, G., Czech, C., Blanchard, V., Multhaup, G., Rezaie, P., et al. (2004) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63235-x · Cited by 281 · see citing works
Self-citationHeikkinen, T., Lehtimäki, K. K., Vartiainen, N. E., Puoliväli, J. T., Hendricks, S. J., Glaser, J. R., Bradaïa, A., Wadel, K., Touller, C., Kontkanen, O., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050717 · Cited by 273 · see citing works
Neurons in the fusiform gyrus are fewer and smaller in autism
van Kooten, I. A. J., Palmen, S. J. M. C., von Cappeln, P., Steinbusch, H. W. M., Korr, H., Heinsen, H., Hof, P. R., van Engeland, H., & Schmitz, C. (2008) · Brain · doi:10.1093/brain/awn033 · Cited by 263 · see citing works
Self-citationSantiago, R. M., Barbieiro, J., Lima, M. M. S., Dombrowski, P. A., Andreatini, R., & Vital, M. A. B. F. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.06.004 · Cited by 251 · see citing works
Slomianka, L., & West, M. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.06.086 · Cited by 236 · see citing works
Nurr1 in Parkinson's disease and related disorders
Chu, Y., Le, W., Kompoliti, K., Jankovic, J. J., Mufson, E. J., & Kordower, J. H. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20828 · Cited by 227 · see citing works
Vereczki, V., Martin, E., Rosenthal, R. E., Hof, P. R., Hoffman, G. E., & Fiskum, G. M. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600234 · Cited by 213 · see citing works
Self-citationSchenker-Ahmed, N. M., Hopkins, W. D., Spocter, M. A., Garrison, A. R., Stimpson, C. D., Erwin, J. M., Hof, P. R., & Sherwood, C. C. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp138 · Cited by 208 · see citing works
Self-citationOximetry-Guided Reoxygenation Improves Neurological Outcome After Experimental Cardiac Arrest
Balan, I. S., Fiskum, G. M., Hazelton, J. L., Cotto-Cumba, C., & Rosenthal, R. E. (2006) · Stroke · doi:10.1161/01.str.0000248455.73785.b1 · Cited by 205 · see citing works
Hao, J., Janssen, W., Tang, Y., Roberts, J. A., McKay, H. M., Lasley, B., Allen, P., Greengard, P., Rapp, P., Kordower, J., et al. (2003) · The Journal of comparative neurology · doi:10.1002/cne.10837 · Cited by 202 · see citing works
Self-citationCao, Q., He, Q., Wang, Y., Cheng, X., Howard, R. M., Zhang, Y., DeVries, W. H., Shields, C. B., Magnuson, D. S. K., Xu, X., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3174-09.2010 · Cited by 203 · see citing works
Molecular and Cellular Evidence for an Oligodendrocyte Abnormality in Schizophrenia
Hof, P. R., Haroutunian, V., Copland, C., Davis, K. L., & Buxbaum, J. D. (2002) · Neurochemical Research · doi:10.1023/a:1020981510759 · Cited by 199 · see citing works
Self-citationTang, Y. C. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg121 · Cited by 197 · see citing works
Volume, neuron density and total neuron number in five subcortical regions in schizophrenia
Kreczmański, P., Heinsen, H., Mantua, V., Woltersdorf, F., Masson, T., Ulfig, N., Schmidt‐Kastner, R., Korr, H., Steinbusch, H. W. M., Hof, P. R., et al. (2007) · Brain · doi:10.1093/brain/awl386 · Cited by 196 · see citing works
Self-citationBussière, T., Giannakopoulos, P., Bouras, C., Perl, D. P., Morrison, J. H., & Hof, P. R. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10760 · Cited by 185 · see citing works
Self-citationWen, P. H., Hof, P. R., Chen, X., Gluck, K., Austin, G., Younkin, S. G., Younkin, L. H., DeGasperi, R., Sosa, M. A. G., Robakis, N. K. R. K., et al. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.04.002 · Cited by 190 · see citing works
Self-citationKozielski, K., Jahanshahi, A., Gilbert, H. B., Yu, Y., Erin, Ö., Francisco, D., Alosaimi, F., Temel, Y., & Sitti, M. (2021) · Science Advances · doi:10.1126/sciadv.abc4189 · Cited by 183 · see citing works
Simms, M. L., Kemper, T. L., Timbie, C. M., Bauman, M. L., & Blatt, G. J. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0568-2 · Cited by 183 · see citing works
Lower motor neuron loss in multiple sclerosis and experimental autoimmune encephalomyelitis
Vogt, J., Paul, F., Aktas, O., Müller-Wielsch, K., Dörr, J., Dörr, S., Bharathi, B. S., Glumm, R., Schmitz, C., Steinbusch, H., et al. (2009) · Annals of Neurology · doi:10.1002/ana.21719 · Cited by 176 · see citing works
Self-citationStereologic investigation of the posterior part of the hippocampus in schizophrenia
Schmitt, A., Steyskal, C., Bernstein, H., Schneider-Axmann, T., Parlapani, E., Schaeffer, E. L., Gattaz, W. F., Bogerts, B., Schmitz, C., & Falkai, P. (2008) · Acta Neuropathologica · doi:10.1007/s00401-008-0430-y · Cited by 167 · see citing works
Self-citationRadley, J. J., Williams, B., & Sawchenko, P. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0552-08.2008 · Cited by 148 · see citing works
Nigrostriatal tau pathology in parkinsonism and Parkinson’s disease
Chu, Y., Hirst, W. D., Federoff, H. J., Harms, A. S., Stoessl, A. J., & Kordower, J. H. (2023) · Brain · doi:10.1093/brain/awad388 · Cited by 149 · see citing works
Preservation of hippocampal neuron numbers in aged rhesus monkeys
Keuker, J. I. H. (2002) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00062-3 · Cited by 141 · see citing works
Nyffeler, M., Meyer, U., Yee, B. K., Feldon, J., & Knuesel, I. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.07.029 · Cited by 139 · see citing works
Schmitz, C., Rhodes, M. E., Bludau, M., Kaplan, S., Ong, P., Ueffing, I., Vehoff, J., Korr, H., & Frye, C. A. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001118 · Cited by 136 · see citing works
Self-citationEarly axonopathy preceding neurofibrillary tangles in mutant tau transgenic mice
Leroy, K., Bretteville, A., Schindowski, K., Gilissen, E., Authelet, M., De Decker, R., Yilmaz, Z., Buée, L., & Brion, J.-P. (2007) · The American Journal of Pathology · doi:10.2353/ajpath.2007.070345 · Cited by 135 · see citing works
Rivara, C., Sherwood, C. C., Bouras, C., & Hof, P. R. (2003) · The Anatomical Record Part A Discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.10015 · Cited by 127 · see citing works
Self-citationCyclin D2 Is Critical for Intermediate Progenitor Cell Proliferation in the Embryonic Cortex
Glickstein, S. B., Monaghan, J. A., Koeller, H. B., Jones, T. K., & Ross, M. E. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2284-09.2009 · Cited by 124 · see citing works
Glickstein, S. B., DeSteno, D. A., Hof, P. R., & Schmauss, C. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh202 · Cited by 122 · see citing works
Self-citationBussire, T., Gold, G., Kvari, E., Giannakopoulos, P., Bouras, C., Perl, D. P., Morrison, J. H., & Hof, P. R. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00942-9 · Cited by 122 · see citing works
Self-citationAlmeida-Suhett, C. P., Prager, E. M., Pidoplichko, V. I., Figueiredo, T. H., Marini, A. M., Li, Z., Eiden, L. E., & Braga, M. F. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102627 · Cited by 117 · see citing works
Temel, Y., Visser-Vandewalle, V. E. R. M., Aendekerk, B., Rutten, B. P. F., Tan, S. K. H., Scholtissen, B., Schmitz, C., Blokland, A., & Steinbusch, H. W. M. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2004.12.025 · Cited by 118 · see citing works
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Glickstein, S. B., Hof, P. R., & Schmauss, C. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05619.2002 · Cited by 119 · see citing works
Self-citationHausdorf, J., Lemmens, M. A. M., Kaplan, S., Marangoz, C., Milz, S., Odacı, E., Korr, H., Schmitz, C., & Maier, M. (2008) · Brain Research · doi:10.1016/j.brainres.2008.02.013 · Cited by 119 · see citing works
Self-citationHazelton, J. L., Balan, I. S., Elmer, G. I., Kristián, T., Rosenthal, R. E., Krause, G. S., Sanderson, T. H., & Fiskum, G. M. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2009.1186 · Cited by 115 · see citing works
Raghanti, M. A., Stimpson, C. D., Marcinkiewicz, J. L., Erwin, J. M., Hof, P. R., & Sherwood, C. C. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.008 · Cited by 114 · see citing works
Self-citationWen, P. H., Shao, X., Shao, Z., Hof, P. R., Wısnıewskı, T., Kelley, K. A., Friedrich, V. L., Ho, L., Pasinetti, G. M., Shioi, J., et al. (2002) · Neurobiology of Disease · doi:10.1006/nbdi.2002.0490 · Cited by 112 · see citing works
Self-citationLehmann, J. (2002) · Neurobiology of Aging · doi:10.1016/s0197-4580(01)00320-7 · Cited by 103 · see citing works
Herculano‐Houzel, S., von Bartheld, C. S., Miller, D. J., & Kaas, J. H. (2015) · Cell and Tissue Research · doi:10.1007/s00441-015-2127-6 · Cited by 103 · see citing works
Cognitive impact of neuronal pathology in the entorhinal cortex and CA1 field in Alzheimer's disease
GUNTEN, A., KOVARI, E., BUSSIERE, T., RIVARA, C., GOLD, G., BOURAS, C., HOF, P., & GIANNAKOPOULOS, P. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.02.008 · Cited by 101 · see citing works
Self-citationMyostatin inhibition slows muscle atrophy in rodent models of amyotrophic lateral sclerosis
Holzbaur, E. L. F., Howland, D., Weber, N., Wallace, K. E., She, Y., Kwak, S., Tchistiakova, L. A., Murphy, E. K., Hinson, J., Karim, R., et al. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.05.009 · Cited by 101 · see citing works
Stereology, morphometry, and mapping: the whole is greater than the sum of its parts
Glaser, J. R., & Glaser, E. M. (2000) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(00)00073-9 · Cited by 100 · see citing works
Navailles, S., Hof, P. R., & Schmauss, C. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21775 · Cited by 97 · see citing works
Self-citationMarcos, R., Monteiro, R. A. F., & Rocha, E. (2012) · Journal of Anatomy · doi:10.1111/j.1469-7580.2012.01475.x · Cited by 95 · see citing works
Prenatal PCBs disrupt early neuroendocrine development of the rat hypothalamus
Dickerson, S. M., Cunningham, S. L., & Gore, A. C. (2011) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2011.01.012 · Cited by 95 · see citing works
Involvement of precerebellar nuclei in multiple system atrophy
Braak, H., Rüb, U., & Tredici, K. D. (2003) · Neuropathology and Applied Neurobiology · doi:10.1046/j.1365-2990.2003.00432.x · Cited by 93 · see citing works
Chakraborty, T. R., Hof, P. R., Ng, L., & Gore, A. C. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10906 · Cited by 94 · see citing works
Self-citationExtensive neuroprotection by choroid plexus transplants in excitotoxin lesioned monkeys
Emerich, D. F., Thanos, C. G., Goddard, M. B., Skinner, S. J. M., Geany, M. S., Bell, W. J., Bintz, B. E., Schneider, P. A., Chu, Y., Babu, R. S., et al. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.04.014 · Cited by 93 · see citing works
Kordower, J. H., Goetz, C. G., Chu, Y., Halliday, G. M., Nicholson, D. A., Musial, T. F., Marmion, D. J., Stoessl, A. J., Sossi, V., Freeman, T. B., et al. (2016) · Annals of Neurology · doi:10.1002/ana.24820 · Cited by 92 · see citing works
Selective cortical interneuron and GABA deficits in cyclin D2-null mice
Glickstein, S. B., Moore, H., Slowinska, B., Racchumi, J., Suh, M., Chuhma, N., & Ross, M. E. (2007) · Development · doi:10.1242/dev.008524 · Cited by 89 · see citing works
Caloric restriction attenuates age-related changes of DNA methyltransferase 3a in mouse hippocampus
Chouliaras, L., van den Hove, D. L. A., Kenis, G., Dela Cruz, J., Lemmens, M. A. M., van Os, J., Steinbusch, H. W. M., Schmitz, C., & Rutten, B. P. F. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.11.016 · Cited by 89 · see citing works
Self-citationAlmeida-Suhett, C. P., Prager, E. M., Pidoplichko, V. I., Figueiredo, T. H., Marini, A. M., Li, Z., Eiden, L. E., & Braga, M. F. M. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.07.028 · Cited by 91 · see citing works
Tong, L., Strong, M. K., Kaur, T., Juiz, J. M., Oesterle, E. C., Hume, C. R., Warchol, M. E., Palmiter, R. D., & Rubel, E. W. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2179-14.2015 · Cited by 89 · see citing works
Chu, Y., Bartus, R. T., Manfredsson, F. P., Olanow, C. W., & Kordower, J. H. (2020) · Brain · doi:10.1093/brain/awaa020 · Cited by 88 · see citing works
Sierksma, A. S. R., Prickaerts, J., Chouliaras, L., Rostamian, S., Delbroek, L., Rutten, B. P. F., Steinbusch, H. W. M., & van den Hove, D. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.05.012 · Cited by 87 · see citing works
Stereologic Analysis of Microvascular Morphology in the Elderly
Bouras, C., Kövari, E., Herrmann, F. R., Rivara, C., Bailey, T. L., von Gunten, A., Hof, P. R., & Giannakopoulos, P. (2006) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/01.jnen.0000203077.53080.2c · Cited by 85 · see citing works
Self-citationHof, P. R., Bussière, T., Gold, G., Kövari, E., Giannakopoulos, P., Bouras, C., Perl, D. P., & Morrison, J. H. (2003) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/62.1.55 · Cited by 85 · see citing works
Self-citationBastide, M. F., Doveró, S., Charron, G., Porras, G., Gross, C. E., Fernagut, P., & Bézard, E. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.09.020 · Cited by 82 · see citing works
Raghanti, M. A., Stimpson, C. D., Marcinkiewicz, J. L., Erwin, J. M., Hof, P. R., & Sherwood, C. C. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm089 · Cited by 81 · see citing works
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Ando, K., Leroy, K., Héraud, C., Yilmaz, Z., Authelet, M., Suain, V., Decker, R. D., & Brion, J. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2010.10.034 · Cited by 80 · see citing works
Vereczki, V., Veres, J. M., Müller, K., Nagy, G. A., Rácz, B., Barsy, B., & Hájos, N. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00020 · Cited by 77 · see citing works
Spencer, S. J., Basri, B., Sominsky, L., Soch, A., Ayala, M. T., Reineck, P., Gibson, B. C., & Barrientos, R. M. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.10.018 · Cited by 80 · see citing works
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Rutten, B. P. F., Schmitz, C., Gerlach, O. H. H., Oyen, H. M., de Mesquita, E. B., Steinbusch, H. W. M., & Korr, H. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.10.019 · Cited by 80 · see citing works
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von Bartheld, C. S. (2017) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2017.08.004 · Cited by 77 · see citing works
Lisney, T. J., Stecyk, K., Kolominsky, J., Schmidt, B. K., Corfield, J. R., Iwaniuk, A. N., & WYLIE, D. R. W. (2013) · Journal of Comparative Physiology A · doi:10.1007/s00359-013-0802-1 · Cited by 76 · see citing works
Koson, P., Žilka, N., Kováč, A., Kováčech, B., Korenova, M., Filipčík, P., & Novák, M. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06329.x · Cited by 75 · see citing works
Chu, Y., Goldman, J. G., Kelly, L. P., He, Y., Waliczek, T., & Kordower, J. H. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.05.003 · Cited by 71 · see citing works
Yurek, D. M., Fletcher‐Turner, A., Kowalczyk, T. H., Padegimas, L., & Cooper, M. J. (2009) · Cell Transplantation · doi:10.3727/096368909x12483162196881 · Cited by 73 · see citing works
Kántor, O., Temel, Y., Holzmann, C., Raber, K. A., Nguyen, H. P., Cao, C., Ozen, H., Rutten, B. P. F., Visser-Vandewalle, V. E. R. M., Steinbusch, H. W. M., et al. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.12.014 · Cited by 73 · see citing works
Self-citationFigueiredo, T. H., Qashu, F. M., Apland, J. P., Aroniadou‐Anderjaska, V., de Souza, A. P., & Braga, M. F. M. (2010) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.110.171835 · Cited by 69 · see citing works
Sherwood, C. C., Raghanti, M. A., Stimpson, C. D., Bonar, C. J., de Sousa, A. A., Preuss, T. M., & Hof, P. R. (2006) · Brain Behavior and Evolution · doi:10.1159/000096986 · Cited by 68 · see citing works
Self-citationSalama, J., Chakraborty, T. R., Ng, L., & Gore, A. C. (2003) · Environmental Health Perspectives · doi:10.1289/ehp.6126 · Cited by 69 · see citing works
Lisney, T. J., Stecyk, K., Kolominsky, J., Graves, G. R., WYLIE, D. R. W., & Iwaniuk, A. N. (2013) · The Anatomical Record · doi:10.1002/ar.22815 · Cited by 67 · see citing works
Apland, J. P., Aroniadou‐Anderjaska, V., Figueiredo, T. H., Rossetti, F., Miller, S. L., & Braga, M. F. M. (2014) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.114.217299 · Cited by 67 · see citing works
Age-Related Changes in Estrogen Receptor β in Rat Hypothalamus: A Quantitative Analysis
Chakraborty, T. R., Ng, L., & Gore, A. C. (2003) · Endocrinology · doi:10.1210/en.2003-0052 · Cited by 66 · see citing works
Rüb, U. (2002) · Brain · doi:10.1093/brain/awf208 · Cited by 66 · see citing works
Damage to the reticulotegmental nucleus of the pons in spinocerebellar ataxia type 1, 2, and 3
Rüb, U., Bürk, K., Schöls, L., Brunt, E., de Vos, R., Díaz, G. O., Gierga, K., Ghebremedhin, E., Schultz, C., Turco, D. D., et al. (2004) · Neurology · doi:10.1212/01.wnl.0000140498.24112.8c · Cited by 58 · see citing works
Raghanti, M. A., Stimpson, C. D., Marcinkiewicz, J. L., ERWIN, J. M., Hof, P. R., & Sherwood, C. C. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21546 · Cited by 62 · see citing works
Self-citationImpact of perinatal asphyxia on the GABAergic and locomotor system
van de Berg, W. D. J., Kwaijtaal, M., de Louw, A. J. A., Lissone, N. P. A., Schmitz, C., Faull, R. L. M., Blokland, A., Blanco, C. E., & Steinbusch, H. W. M. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00787-x · Cited by 62 · see citing works
Self-citationTotal Number and Ratio of GABAergic Neuron Types in the Mouse Lateral and Basal Amygdala
Vereczki, V., Müller, K., Krizsán, É., Máté, Z., Fekete, Z., Rovira-Esteban, L., Veres, J. M., Erdélyi, F., & Hájos, N. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2700-20.2021 · Cited by 60 · see citing works
Practical approaches to stereology in the setting of aging- and disease-related brain banks
Perl, D. P., Good, P. F., Bussière, T., Morrison, J. H., ERWIN, J. M., & Hof, P. R. (2000) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(00)00077-6 · Cited by 61 · see citing works
Self-citationWu, D., & Gore, A. C. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.001 · Cited by 61 · see citing works
The revolution of counting “tops”: Two decades of the disector principle in morphological research
Geuna, S. (2005) · Microscopy Research and Technique · doi:10.1002/jemt.20167 · Cited by 60 · see citing works
Fritsch, B., Qashu, F. M., Figueiredo, T. H., Aroniadou‐Anderjaska, V., Rogawski, M. A., & Braga, M. F. M. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.06.034 · Cited by 60 · see citing works
Prager, E. M., Aroniadou‐Anderjaska, V., Almeida-Suhett, C. P., Figueiredo, T. H., Apland, J. P., Rossetti, F., Olsen, C. H., & Braga, M. F. M. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.01.035 · Cited by 59 · see citing works
Luo, Y., Xiao, Q., Wang, J., Jiang, L. H., Hu, M., Jiang, Y., Tang, J., Liang, X., Qi, Y., Dou, X., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0662-8 · Cited by 57 · see citing works
Upadhaya, A. R., Capetillo‐Zarate, E., Kosterin, I., Abramowski, D., Kumar, S., Yamaguchi, H., Walter, J., Fändrich, M., Staufenbiel, M., & Thal, D. R. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.12.032 · Cited by 54 · see citing works
Willard, S. L., Riddle, D. R., Forbes, M. E., & Shively, C. A. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.03.013 · Cited by 54 · see citing works
Update on stereology for light microscopy
Geuna, S., & Herrera‐Rincon, C. (2015) · Cell and Tissue Research · doi:10.1007/s00441-015-2143-6 · Cited by 54 · see citing works
Cartwright, N. D., Hardie, J., Montuschi, E., Soleiman, M., & Thresher, A. C. (2022) · doi:10.1093/oso/9780198866343.001.0001 · Cited by 52 · see citing works
Prager, E. M., Aroniadou‐Anderjaska, V., Almeida-Suhett, C. P., Figueiredo, T. H., Apland, J. P., & Braga, M. F. M. (2013) · NeuroToxicology · doi:10.1016/j.neuro.2013.06.006 · Cited by 52 · see citing works
- Authors
- Schmitz, C., & Hof, P. R.
- Affiliations
- RWTH Aachen University (DE)
- Icahn School of Medicine at Mount Sinai (US)
- Corresponding author
- Schmitz, Christoph
- Venue
- Journal of Chemical Neuroanatomy
- Publisher
- Elsevier BV
- Published
- 2000-10
- Volume
- 20
- Issue
- 1
- Pages
- 93-114
- ISSN
- 0891-0618 (ISSN-L)
- OpenAlex
- W2168092251
- Cited by
- 272
- References
- 53
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 1 · 2023: 5 · 2022: 22 · 2021: 6 · 2020: 8 · 2019: 4 · 2018: 12 · 2017: 6 · 2016: 10 · 2015: 11 · 2014: 11 · 2013: 11 · 2012: 16
- FWCI
- 23.64
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Chemical Neuroanatomy (publishedVersion)
- PubMed (publishedVersion)
- RWTH Publications (RWTH Aachen) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (AG-02219, AG 05138, P50AG005138, P01AG002219)
- National Institute of Mental Health (MH-58911, P50MH058911)
- Topics
- Physical Sciences › Mathematics › Applied Mathematics › Point processes and geometric inequalities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Cell Image Analysis Techniques
- Physical Sciences › Mathematics › Statistics and Probability › Census and Population Estimation
- Keywords
- neuron counting, design-based stereology, neuronal density, coefficient of variation, estimation precision
- MeSH terms
- Algorithms, Brain, Cell Count, Computer Simulation, Image Interpretation, Computer-Assisted, Models, Neurological, Terminology as Topic, Random Allocation
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