Unbiased stereological estimation of the number of neurons in the human hippocampus
Abstract
The total numbers of neurons in five subdivisions of human hippocampi were estimated using unbiased Stereological principles and systematic sampling techniques. The method addresses the problems associated with the results and conclusions of previous quantitative studies, virtually all of which have been based on biased estimates of neuron densities. For each subdivision, the total number of neurons was calculated as the product of the estimate of the volume of the neuron‐containing layers and the estimate of the numerical density of neurons in the layers. Each hippocampus was cut into 3‐mm‐thick slabs, transverse to the rostrocaudal axis. One 70‐μUm‐thick section from each slab was used in the analysis. The volumes of the layers containing neurons in five major subdivisions of the hippocampus (granule cell layer, hilus, CA3–2, CA1, and subiculum) were estimated with point‐counting techniques after delineation of the layers on each section. The numerical densities of neurons in each subdivision were estimated on the same sections with optical directors. The sampling used in both estimates was performed systematically in all three dimensions. In an example of five hippocampi, the mean numbers of neurons (CV = SD/mean) in the different subdivisions were as follows: granule cells 15 × 10 6 (0.28), hilus 2.0 × 10 6 (0.16), CA3‐2 2.7 × 10 6 (0.22), CA1 16 × 10 6 (0.32), subiculum 4.5 × 10 6 (0.19). The stereological measurements contributed approximately 25% of the observed variance. Among the five subjects there was a significant inverse relationship between age (which ranged from 47 to 85 years) and the total number of neurons in CA1 (which ranged from 24 to 11 × 10 6). An optimized sampling scheme for studies of the number of neurons in the human hippocampus has been designed on the basis of an analysis of variance of the estimates at different levels of the sampling scheme. Counting neurons in the five subdivisions of the human hippocampus with the optimized sampling scheme takes less than 4 hours.
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Coefficients of error were calculated as estimates of precision; values were 0.047 ± 0.006667 for pSer-129+ cells and 0.063 ± 0.012 for GFP+ cells in NHPs, and 0.105 ± 0.0087 for GFP+ cells in rats.
“The coefficients of error (CE) were calculated according to the procedure of Gunderson and colleagues as estimates of precision [66]. The values of CE were 0.047 ± 0.006667 (Gunndersen m = 0) for pSer-129+ cells and 0.063 ± 0.012 (Gunndersen m = 0) for GFP+ cells in NHPs, and 0.105 ± 0.0087 GFP+ cells for rats.”
From Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodents and nonhuman primates (2017) · cites this paper as [66]
Stereological counting methods using the optical fractionator probe in Stereo Investigator were applied to estimate GFP+ or pSer-129+ cells in rats and monkeys in an unbiased fashion.
“In order to estimate the number cells transduced by Olig001, GFP+ or pSer-129+ cells in rats and monkeys in an unbiased fashion, stereological counting methods [66] using the optical fractionator probe in Stereo Investigator (Microbrightfield Bioscience, Version10.40) were applied.”
From Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodents and nonhuman primates (2017) · cites this paper as [66]
The first section plane was placed randomly to ensure unbiased estimation.
“To ensure that the estimation was unbiased, the first section plane was placed randomly within the first interval length (West and Gundersen, 1990).”
From Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer’s Disease (1996) · cites this paper as West and Gundersen, 1990
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“Thus, utilization of the Giemsa stain predates the adoption of this stain by Gundersen, West, and Pakkenberg for their resin sections in the 1980s and 1990s (e.g., Gundersen et al., 1988; West and Gundersen, 1990; Regeur et al., 1994a).”
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“We then employed standard stereological procedures to estimate the areal and laminar density of boutons, using the optical fractionator according to the method described by West and Gundersen (e.g., Gundersen et al., 1988; West and Gundersen, 1990).”
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“Interestingly, it was recently reported (West and Gundersen, 1990) that, when correcting appropriately for postmortem shrinkage of tissues, the numbers for humans increase to 15 x 106 :t 28% (DG), 2.7 x 106 :t 22% (CA3), and 16 x 166 :t 32% (CAl). tex, make synapses on the apical dendrites of CA3…”
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“Estimated total numbers of neurons within a BROI can be obtained by the " V Ref ϫN V " method (West and Gundersen , 1990), i.e. by calculating the product of the mean neuron density within the unbiased virtual counting spaces (N V ) and the global volume of the BROI (V Ref ; estimated with…”
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“Neuron counts were performed using the optical disector technique (West and Gundersen, 1990) in 40 mM cresyl violet-stained coronal sections spaced 240 mM apart.”
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“…aging and disease showed normal individuals to lose neurons in two regions of the hippocampus, subiculum and the hilus as a function of age, while patients with AD lost more neurons in these two regions than normal aging individuals (West and Gundersen, 1990; West et al., 1994; Simic et al., 1997).”
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“7 million pyramidal neurons in the CA2-3 region, plus ~2 million neurons located in the hilus [112].”
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“Stereologically-based counts of neurofibrillary tangles, neurons, GFAP-positive astrocytes and CD68-positive microglial cells were performed as previously described (West and Gundersen, 1990; Gomez-Isla et al., 1996).”
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“The coefficients of error (CE) were calculated according to the procedure of Gunderson and colleagues as estimates of precision (West and Gundersen, 1990; Schmitz and Hof, 2000).”
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“Unbiased stereological techniques (Gundersen et al., 1988; West & Gundersen, 1990; West, 1999) were used to estimate cell number in the substantia nigra pars compacta (SNc).”
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“The coefficient of error (SD/mean) (Gundersen and Jensen, 1987; West and Gundersen, 1990) was Ͻ0.”
BackgroundConsequences of neonatal seizures in the rat: Morphological and behavioral effects
Gl, H., Gairsa, J., Chevassus-au-Louis, N., & Ben‐Ari, Y. (1998) · Annals of Neurology · doi:10.1002/ana.410440602 · Cited by 388 · see citing works
Boldrini, M., Santiago, A. N., Hen, R., Dwork, A. J., Rosoklija, G. B., Tamir, H., Arango, V., & John Mann, J. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.5 · Cited by 361 · see citing works
A novel GSK-3β inhibitor reduces Alzheimer's pathology and rescues neuronal loss in vivo
Serenó, L., Coma, M., Rodríguez, M., Sánchez-Ferrer, P., Sánchez, M. B., Gich, I., Agulló, J. M., Pérez, M., Avila, J., Guardia-Laguarta, C., et al. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.05.025 · Cited by 368 · see citing works
Complement<i>C3</i>-Deficient Mice Fail to Display Age-Related Hippocampal Decline
Shi, Q., Colodner, K. J., Matousek, S. B., Merry, K., Hong, S., Kenison, J. E., Frost, J. L., Le, K. X., Li, S., Dodart, J.-C., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1698-15.2015 · Cited by 368 · see citing works
“The number of neurons per section in each brain region was estimated using 15 optical dissectors and the Bioquant image analysis system according to the principles of Cavalieri (West and Gundersen, 1990).”
MethodSelective clearance of aberrant tau proteins and rescue of neurotoxicity by transcription factor EB
Polito, V. A., Li, H., Martini‐Stoica, H., Wang, B., Li, Y., Xu, Y., Swartzlander, D. B., Palmieri, M., di Ronza, A., Lee, V. M. ‐., et al. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201303671 · Cited by 350 · see citing works
Bordi, M., Berg, M. J., Mohan, P. S., Peterhoff, C. M., Alldred, M. J., Che, S., Ginsberg, S. D., & Nixon, R. A. (2016) · Autophagy · doi:10.1080/15548627.2016.1239003 · Cited by 353 · see citing works
Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage
Jones, T. A., & Schallert, T. J. (1992) · Brain Research · doi:10.1016/0006-8993(92)90356-e · Cited by 346 · see citing works
Isgor, C., Kabbaj, M., Akil, H., & Watson, S. J. (2004) · Hippocampus · doi:10.1002/hipo.10207 · Cited by 341 · see citing works
“The coefficient of variation was determined as described by West and Gundersen (1990) and was reported with the neuronal count estimates below.”
MethodDong, H., Goico, B., Martin, M., Csernansky, C. A., Bertchume, A., & Csernansky, J. G. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.05.040 · Cited by 342 · see citing works
Mitochondrial function and morphology are impaired in parkin‐mutant fibroblasts
Mortiboys, H., Craig, K. J. T., Koopman, W. J. H., Klaffke, S., Abou‐Sleiman, P. M., Olpin, S. E., Wood, N. W., Willems, P. H. G. M., Smeitink, J. A. M., Cookson, M., et al. (2008) · Annals of Neurology · doi:10.1002/ana.21492 · Cited by 339 · see citing works
Maier, M., Peng, Y., Jiang, L., Seabrook, T. J., Carroll, M. C., & Lemere, C. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0829-08.2008 · Cited by 323 · see citing works
“The average number of neurons per section in the CA3 region of hippocampus was estimated using 12 optical dissectors and the Bioquant Image Analysis System according to the principle of Cavalieri (West and Gundersen, 1990).”
MethodLeptin signaling in astrocytes regulates hypothalamic neuronal circuits and feeding
Kim, J. G., Suyama, S., Koch, M., Jin, S., Argente-Arizon, P., Argente, J., Liu, Z.-W., Zimmer, M. R., Jeong, J. K., Szigeti-Buck, K., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3725 · Cited by 336 · see citing works
Kolkova, K., Novitskaya, V., Pedersen, N. M., Berezin, V., & Bock, E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-06-02238.2000 · Cited by 330 · see citing works
A review of recent advances in stereology for quantifying neural structure
Mayhew, T. M. (1992) · Journal of Neurocytology · doi:10.1007/bf01191700 · Cited by 330 · see citing works
Age-induced white matter changes in the human brain: a stereological investigation.
Tang, Y., Nyengaard, J., Pakkenberg, B., & Gundersen, H. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00155-3 · Cited by 345 · see citing works
Self-citationHippocampal neurons in pre-clinical Alzheimer's disease.
West, M. J., Kawas, C. H., Stewart, W. F., Rudow, G. L., & Troncoso, J. C. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2003.12.005 · Cited by 317 · see citing works
“method combines fractionator sampling [12] with optical disector counting[13,37].”
MethodSelf-citationThe pre-mild cognitive impairment, subjective cognitive impairment stage of Alzheimer’s disease.
Reisberg, B., Prichep, L., Mosconi, L., John, E. R., Glodzik‐Sobanska, L., Boksay, I., Monteiro, I., Torossian, C., Vedvyas, A., Ashraf, N., et al. (2008) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2007.11.017 · Cited by 312 · see citing works
Geinisman, Y., deToledo‐Morrell, L., Morrell, F., & Heller, R. E. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(94)00047-l · Cited by 317 · see citing works
Subregional hippocampal atrophy predicts Alzheimer's dementia in the cognitively normal
Apostolova, L. G., Mosconi, L., Thompson, P. M., Green, A. E., Hwang, K., Ramírez, A., Mistur, R. L., Tsui, W. H., & de Leon, M. J. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.08.008 · Cited by 313 · see citing works
“Thus our conclusions in respect to selective subeld involvement are based on assumptions about the location f each subfield boundary made in consultation with two ell-established hippocampal histologic atlases (Duvernoy, 988; West and Gundersen, 1990).”
BackgroundMethodYücel, Y. H. (2000) · Archives of Ophthalmology · doi:10.1001/archopht.118.3.378 · Cited by 305 · see citing works
“Stereological procedures that provide unbiased estimates of cell numbers were used.(19-22) Neurozoom software (Human Brain Project, La Jolla Calif) enabled digital superposition of the sampling grids on the tissue.”
Le, D. A., Wu, Y., Huang, Z., Matsushita, K., Plesnila, N., Augustinack, J. C., Hyman, B. T., Yuan, J., Kuida, K., Flavell, R. A., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.232473399 · Cited by 303 · see citing works
Hippocampal interneurons are abnormal in schizophrenia
Konradi, C., Yang, C. K., Zimmerman, E. I., Lohmann, K. M., Gresch, P., Pantazopoulos, H., Berretta, S., & Heckers, S. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.06.007 · Cited by 288 · see citing works
“Each human hippocampus contains approximately 10 million neurons, of which 90% are large, pyramidal-shaped, glutamatergic neurons and the remaining 10% are small, non-pyramidal, gammaamino-butyric acid (GABA)ergic neurons (Olbrich and Braak, 1985; West and Gundersen, 1990; Freund and Buzsaki, 1996).”
Pitx3 is required for motor activity and for survival of a subset of midbrain dopaminergic neurons
van den Munckhof, P., Luk, K. C., Ste‐Marie, L., Montgomery, J. A., Blanchet, P. J., Sadikot, A. F., & Drouin, J. (2003) · Development · doi:10.1242/dev.00464 · Cited by 300 · see citing works
“Unbiased estimates of midbrain DA neurons were obtained using the optical dissector method of West and Gundersen (West and Gundersen, 1990; West, 1993).”
Popken, G. J., & Farel, P. B. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970915)386:1 · Cited by 117 · see citing works
Crews, F. T., Qin, L., Sheedy, D. L., Vetreno, R. P., & Zou, J. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.09.030 · Cited by 295 · see citing works
Savage, M. J., Lin, Y.-G., Ciallella, J. R., Flood, D. G., & Scott, R. W. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03376.2002 · Cited by 291 · see citing works
“Neurons were counted with the CASTGrid System (Olympus Optical, Denmark, Copenhagen) using the optical dissector technique (West and Gundersen, 1990).”
MethodMayhew, T. M., & Gundersen, H. J. G. (1996) · PubMed · Cited by 291 · see citing works
Self-citationLivy, D. J., Miller, E. K., Maier, S. E., & West, J. R. (2003) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(03)00030-8 · Cited by 290 · see citing works
Qin, L., & Crews, F. T. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-5 · Cited by 290 · see citing works
“optical disector method [34,35], which was calculated as follows:”
MethodPyramidal cell regulation of interneuron survival sculpts cortical networks
Wong, F. K., Bercsenyi, K., Sreenivasan, V., Portalés, A., Fernández-Otero, M., & Marín, O. (2018) · Nature · doi:10.1038/s41586-018-0139-6 · Cited by 286 · see citing works
Samuelsson, A., Jennische, E., Hansson, H., & Holmäng, A. B. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00268.2005 · Cited by 283 · see citing works
“Neuronal density in the hilus, CA1, CA2, and CA3 regions was estimated as the average percentage of Nissl-stained neurons in five counting frames (50 50 m) distributed systematically and randomly in the study area, as described previously (62).”
MethodAge-related differences in the functional connectivity of the hippocampus during memory encoding
Grady, C. L., McIntosh, A. R., & Craik, F. I. M. (2003) · Hippocampus · doi:10.1002/hipo.10114 · Cited by 277 · see citing works
“For example, one study reported a loss of neurons in CA1 and subiculum with age, but not in other subdivisions of the hippocampus (Simic et al., 1997).”
BackgroundStein, T. D., Anders, N. J., DeCarli, C. S., Chan, S. L., Mattson, M. P., & Johnson, J. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2211-04.2004 · Cited by 276 · see citing works
“Every sixth section was stained with cresyl violet , and neurons with healthy and intact nuclei were counted within the cornu ammonis 1 ( CA1 ) pyramidal neuronal field using the optical fractionator technique ( West and Gundersen , 1990 ) .”
MethodA quantitative study of the human cerebellum with unbiased stereological techniques
Andersen, B. B., Korbo, L., & Pakkenberg, B. (1992) · Journal of Comparative Neurology · doi:10.1002/cne.903260405 · Cited by 276 · see citing works
Schmitz, C., & Hof, P. R. (2000) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(00)00066-1 · Cited by 272 · 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.”
BackgroundMethodInfluentialContestabile, A., Fila, T., Ceccarelli, C., Bonasoni, P., Bonapace, L., Santini, D., Bartesaghi, R., & Ciani, E. (2007) · Hippocampus · doi:10.1002/hipo.20308 · Cited by 281 · see citing works
“In P30 animals, granule cell density (NV) in the granule cell layer of the DG was stereologically (West and Gundersen, 1990) determined in NeuN-stained section, by counting in one out of every 12 sections the number of granule cells present in dissectors with dimensions of 25 lm 3 25 lm 3 10 lm,…”
Guidi, S., Bonasoni, P., Ceccarelli, C., Santini, D., Gualtieri, F., Ciani, E., & Bartesaghi, R. (2008) · Brain Pathology · doi:10.1111/j.1750-3639.2007.00113.x · Cited by 276 · see citing works
“Based on the Cavalieri principle (17, 52), we estimated the reference volume (Vref) of the granule cell layer, pyramidal layer, lamina principalis interna and lamina principalis externa of the PRES and EC and single cellular lamina of the LPHG by multiplying the sum of the areas measured in the series of sections by t…”
MethodВитальевич, П. В., & Clayton, N. S. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.4.515 · Cited by 256 · see citing works
“In accordance with the Cavalieri principle (Gundersen & Jensen, 1987; West & Gundersen, 1990 ), we chose the first section randomly from the first 4 sections containing the hippocampus.”
MethodInfluentialWagner, 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
Self-citationBergmann, O., Spalding, K. L., & Frisén, J. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018994 · Cited by 256 · see citing works
Mapping local hippocampal changes in Alzheimer's disease and normal ageing with MRI at 3 Tesla
Frisoni, G. B., Ganzola, R., Canu, E., Rub, U., Pizzini, F. B., Alessandrini, F., Zoccatelli, G., Beltramello, A., Caltagirone, C., & Thompson, P. M. (2008) · Brain · doi:10.1093/brain/awn280 · Cited by 256 · see citing works
“For example, pyramidal cells are lost in the subiculum between age 30 and 60 years (Trillo and Gonzalo, 1992), but stabilize thereafter (West and Gundersen, 1990; Trillo and Gonzalo, 1992), while cell loss in the presubiculum and CA1 subfield is more linearly associated with increasing age at least…”
BackgroundReceptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain
Anton, E. S., Ghashghaei, H. T., Weber, J. L., McCann, C. M., Fischer, T. M., Cheung, I. D., Gassmann, M., Messing, A., Klein, R., Schwab, M. H., et al. (2004) · Nature Neuroscience · doi:10.1038/nn1345 · Cited by 256 · see citing works
“The numbers of calbindin + , calretinin + and GAD65 + cells in the periglomerular layer of the OB were estimated using the optical fractionator metho”
3D comparison of hippocampal atrophy in amnestic mild cognitive impairment and Alzheimer's disease
Apostolova, L. G., Dinov, I. D., Dutton, R. A., Hayashi, K. M., Toga, A. W., Cummings, J. L., & Thompson, P. M. (2006) · Brain · doi:10.1093/brain/awl274 · Cited by 251 · see citing works
“A schematic of subregional hippocampal anatomy in 3D was prepared in consultation with two wellestablished sources (Duvernoy, 1988; West and Gundersen, 1990) (Fig.”
MethodCarlton, S. M., Du, J., Tan, H. Y., Nešić, O., Hargett, G. L., Bopp, A. C., Yamani, A., Lin, Q., Willis, W. D., & Hulsebosch, C. E. (2009) · Pain · doi:10.1016/j.pain.2009.09.030 · Cited by 251 · see citing works
“Using ‘‘fractionator sampling” [28,93], total numbers of cresyl violet stained neurons and numbers of ATF3-labeled neurons were estimated by multiplying ‘‘Q-” by the reciprocal of the fraction (1/f) of each sampled section pair.”
MethodFreese, J. L., & Amaral, D. G. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20945 · Cited by 242 · see citing works
“The volumes of these boutons were measured according to the Cavalieri principal (Gundersen and Jensen, 1987; West and Gundersen, 1990).”
MethodInsausti, R., & Amaral, D. G. (2004) · Elsevier eBooks · doi:10.1016/b978-012547626-3/50024-7 · Cited by 246 · see citing works
Smith, D. E., Roberts, J. A., Gage, F. H., & Tuszynski, M. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.19.10893 · Cited by 244 · see citing works
Feature article: are neurons lost from the primate cerebral cortex during normal aging?
Peters, A. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.4.295 · Cited by 245 · see citing works
“Initially the study concentrated on the CA1 and subicular subfields because of the prominent cell loss reported there in humans (West and Gundersen, 1990) and monkeys (Brizzee et al., 1980).”
BackgroundQuantitative Architecture Distinguishes Prefrontal Cortical Systems in the Rhesus Monkey
Dombrowski, S. M. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.10.975 · Cited by 240 · see citing works
“The density of neurons and glia was estimated using a counting method adapted from previous studies (Sterio, 1984; Braendgaard and Gundersen, 1986; Williams and Rakic, 1988; Gundersen et al., 1988; West and Gundersen, 1990; West, 1993) [for a review see (Coggeshall and Lekan, 1996)].”
MethodCorrelates of hippocampal neuron number in Alzheimer's disease and ischemic vascular dementia
Zarow, C., Vinters, H. V., Ellis, W. G., Weiner, M. W., Mungas, D., White, L., & Chui, H. C. (2005) · Annals of Neurology · doi:10.1002/ana.20503 · Cited by 241 · see citing works
“One gallocyanine-stained section was systematically chosen from each slab, and the CA1 and CA2 regions were identified and outlined on the coverslip using waterproof markers.(17) The slide was placed on the microscope stage in a random orientation and overlaid with a uniform grid.”
Methodvan Boxel-Dezaire, A. H. H., Hoff, S. C. J., van Oosten, B. W., Verweij, C. L., Dräger, A. M., Adèr, H. J., van Houwelingen, H. C., Barkhof, F., Polman, C. H., & Nagelkerken, L. M. (1999) · Annals of Neurology · doi:10.1002/1531-8249(199906)45:6 · Cited by 266 · see citing works
Redila, V. A., & Christie, B. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.050 · Cited by 235 · see citing works
“This represents some 6% of a structure that is stimated to be composed of some 2.4 million neurons Cameron and McKay, 2001; West and Gundersen, 1990). oreover, the number of new neurons being produced is ikely much larger in animals that exercise (Eadie et al., 005).”
BackgroundInfluentialAnnese, J., Schenker-Ahmed, N. M., Bartsch, H., Maechler, P., Sheh, C., Thomas, N., Kayano, J., Ghatan, A., Bresler, N., Frosch, M. P., et al. (2014) · Nature Communications · doi:10.1038/ncomms4122 · Cited by 234 · see citing works
“Additional quantitative analyses involving unbiased stereological methods can provide information regarding neuronal size and number 43 in this region.”
MethodTakeuchi, A., Irizarry, M. C., Duff, K., Saido, T. C., Hsiao Ashe, K., Hasegawa, M., Mann, D. M. A., Hyman, B. T., & Iwatsubo, T. (2000) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)64544-0 · Cited by 229 · see citing works
Oxygen causes cell death in the developing brain
Felderhoff‐Mueser, U., Bittigau, P., Sifringer, M., Jarosz, B., Korobowicz, E. M., Mahler, L., Piening, T., Moysich, A., Grune, T., Thor, F., et al. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.07.019 · Cited by 229 · see citing works
Layer I of primary sensory neocortex: where top-down converges upon bottom-up
Cauller, L. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00032-1 · Cited by 225 · see citing works
Young, K. G., Chang, J. P., & Goldberg, J. I. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990222)404:4 · Cited by 68 · see citing works
- Authors
- West, M. J., & Gundersen, H. J. G.
- Affiliations
- Aarhus University (DK)
- Corresponding author
- West, Mark J.
- ORCID
- West, Mark J.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1990-06
- Volume
- 296
- Issue
- 1
- Pages
- 1-22
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2014892312
- Cited by
- 1,153
- References
- 47
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 10 · 2023: 17 · 2022: 24 · 2021: 22 · 2020: 24 · 2019: 19 · 2018: 40 · 2017: 27 · 2016: 32 · 2015: 30 · 2014: 38 · 2013: 40 · 2012: 41
- FWCI
- 46.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Sundhed og Sygdom, Det Frie Forskningsråd
- Topics
- Physical Sciences › Mathematics › Applied Mathematics › Point processes and geometric inequalities
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Anatomy › Medical and Biological Sciences
- Keywords
- human hippocampus, neuron number estimation, neuronal density, unbiased stereology, optical disector, point counts, CA1, CA3, subiculum, granular layer, hilus, age-related neuronal loss
- MeSH terms
- Aged, Aged, 80 and over, Cell Count, Hippocampus, Humans, Middle Aged
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